Ultrasound characterization for thyroid nodules with indeterminate cytology: inter-observer agreement and impact of combining pattern-based and scoring-based classifications in risk stratification
- 22 Downloads
The American Thyroid Association (ATA) sonographic patterns stratify the risk of malignancy of cytologically indeterminate thyroid nodules (ITNs). This study aimed to (1) assess inter-observer agreement for sonographic features and patterns; (2) identify potential sources of disagreement; and (3) evaluate whether the number of suspicious features risk-stratifies non-ATA and high-suspicion patterns.
Three observers independently reviewed the ultrasound images of 463 ITNs with histological follow-up consecutively evaluated between October 2008 and June 2015 at an academic cancer center. Each observer evaluated individual sonographic features. ATA sonographic patterns were derived from the interpretation of sonographic features. Nodules not fitting into any of the proposed patterns were clustered into a non-ATA pattern.
The inter-observer agreement for ATA sonographic patterns and echogenicity was fair, moderate for margins, good for composition and echogenic foci, and very good for extrathyroidal extension and lymph node metastasis. The interpretation of each sonographic feature was significantly different between observers, and there was complete disagreement in at least one of the features in 104 (22%) nodules. A total of 169 nodules (37%) were classified into the non-ATA pattern. The number of suspicious features allowed risk stratifying nodules with non-ATA and high-suspicion sonographic patterns. Most Non-invasive Follicular Thyroid Neoplasms with Papillary-like Nuclear Features had 0–1 suspicious features and none had >2.
Echogenicity interpretation was the greatest source of disagreement. The number of suspicious features risk-stratifies ITNs with non-ATA or high-suspicion patterns. Future studies attempting to objectivize the interpretation of echogenicity and heterogeneity are needed.
KeywordsThyroid ultrasound Thyroid cytology Thyroid nodules Thyroid cancer Non-invasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP)
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
The study was carried with a waiver of informed consent from our Institutional Review Board.
- 5.J.P. Zevallos, C.M. Hartman, J.R. Kramer, E.M. Sturgis, E.Y. Chiao, Increased thyroid cancer incidence corresponds to increased use of thyroid ultrasound and fine-needle aspiration: a study of the Veterans Affairs health care system. Cancer 121(5), 741–746 (2015). https://doi.org/10.1002/cncr.29122 Google Scholar
- 7.B.R. Haugen, E.K. Alexander, K.C. Bible, G.M. Doherty, S.J. Mandel, Y.E. Nikiforov, F. Pacini, G.W. Randolph, A.M. Sawka, M. Schlumberger, K.G. Schuff, S.I. Sherman, J.A. Sosa, D.L. Steward, R.M. Tuttle, L. Wartofsky, 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 26(1), 1–133 (2016). https://doi.org/10.1089/thy.2015.0020 Google Scholar
- 8.P. Campanella, F. Ianni, C.A. Rota, S.M. Corsello, A. Pontecorvi, Quantification of cancer risk of each clinical and ultrasonographic suspicious feature of thyroid nodules: a systematic review and meta-analysis. Eur. J. Endocrinol. / Eur. Fed. Endocr. Soc. 170(5), R203–R211 (2014). https://doi.org/10.1530/eje-13-0995 Google Scholar
- 10.J.P. Brito, M.R. Gionfriddo, A. Al Nofal, K.R. Boehmer, A.L. Leppin, C. Reading, M. Callstrom, T.A. Elraiyah, L.J. Prokop, M.N. Stan, M.H. Murad, J.C. Morris, V.M. Montori, The accuracy of thyroid nodule ultrasound to predict thyroid cancer: systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 99(4), 1253–1263 (2014). https://doi.org/10.1210/jc.2013-2928 Google Scholar
- 13.P. Valderrabano, D.L. Klippenstein, J.B. Tourtelot, Z. Ma, Z.J. Thompson, H.S. Lilienfeld, B. McIver, New American Thyroid Association Sonographic Patterns for Thyroid Nodules Perform Well in Medullary Thyroid Carcinoma: Institutional Experience, Systematic Review, and Meta-Analysis. Thyroid 26(8), 1093–1100 (2016). https://doi.org/10.1089/thy.2016.0196 Google Scholar
- 14.P. Valderrabano, M.J. McGettigan, C.A. Lam, L. Khazai, Z.J. Thompson, C.H. Chung, B.A. Centeno, B. McIver, Thyroid nodules with indeterminate cytology: utility of the American Thyroid Association Sonographic Patterns for Cancer Risk Stratification. Thyroid 28(8), 1004–1012 (2018). https://doi.org/10.1089/thy.2018.0085 Google Scholar
- 16.Randolph, J. Free-marginal multirater kappa: an alternative to Fleiss’ fixed-marginal multirater kappa. Joensuu University Learning and Instruction Symposium, Joensuu, Finland, 2005.Google Scholar
- 21.W. Phuttharak, A. Boonrod, V. Klungboonkrong, T. Witsawapaisan, Interrater Reliability of Various Thyroid Imaging Reporting and Data System (TIRADS) Classifications for Differentiating Benign from Malignant Thyroid Nodules. Asian Pac. J. Cancer Prev. 20(4), 1283–1288 (2019). https://doi.org/10.31557/APJCP.2019.20.4.1283 Google Scholar
- 23.P. Trimboli, M. Deandrea, A. Mormile, L. Ceriani, F. Garino, P.P. Limone, L. Giovanella, American Thyroid Association ultrasound system for the initial assessment of thyroid nodules: use in stratifying the risk of malignancy of indeterminate lesions. Head. Neck 40(4), 722–727 (2018). https://doi.org/10.1002/hed.25038 Google Scholar
- 24.T.G. Rocha, P.W. Rosario, A.L. Silva, M.B. Nunes, T.H. Silva, P.H.L. de Oliveira, M.R. Calsolari, Ultrasonography Classification of the American Thyroid Association for Predicting Malignancy in Thyroid Nodules >1cm with Indeterminate Cytology: A Prospective Study. Horm. Metab. Res 50(8), 597–601 (2018). https://doi.org/10.1055/a-0655-3016 Google Scholar
- 25.G. Grani, M. D’Alessandri, G. Carbotta, A. Nesca, M. Del Sordo, S. Alessandrini, C. Coccaro, R. Rendina, M. Bianchini, N. Prinzi, A. Fumarola, Grey-scale analysis improves the ultrasonographic evaluation of thyroid nodules. Med. (Baltim.) 94(27), e1129 (2015). https://doi.org/10.1097/MD.0000000000001129 Google Scholar
- 26.L. Gao, X. Xi, J. Wang, X. Yang, Y. Wang, S. Zhu, X. Lai, X. Zhang, R. Zhao, B. Zhang, Ultrasound risk evaluation of thyroid nodules that are “unspecified” in the 2015 American Thyroid Association management guidelines: a retrospective study. Med. (Baltim.) 97(52), e13914 (2018). https://doi.org/10.1097/MD.0000000000013914 Google Scholar
- 27.J.E. Lim-Dunham, I. Erdem Toslak, K. Alsabban, A. Aziz, B. Martin, G. Okur, K.C. Longo, Ultrasound risk stratification for malignancy using the 2015 American Thyroid Association Management Guidelines for Children with Thyroid Nodules and Differentiated Thyroid Cancer. Pedia. Radio. 47(4), 429–436 (2017). https://doi.org/10.1007/s00247-017-3780-6 Google Scholar
- 28.G. Grani, L. Lamartina, V. Ascoli, D. Bosco, F. Nardi, F. D’Ambrosio, A. Rubini, L. Giacomelli, M. Biffoni, S. Filetti, C. Durante, V. Cantisani, Ultrasonography scoring systems can rule out malignancy in cytologically indeterminate thyroid nodules. Endocrine 57(2), 256–261 (2017). https://doi.org/10.1007/s12020-016-1148-6 Google Scholar