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Ultrasonography scoring systems can rule out malignancy in cytologically indeterminate thyroid nodules

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Abstract

Purpose

To assess the accuracy and reproducibility of ultrasonography classification systems in characterizing cytologically indeterminate thyroid nodules.

Methods

We retrospectively identified 49 nodules that had been surgically resected owing to features classified as indeterminate according to 2010 Italian Consensus on Thyroid Cytology criteria. Three experienced sonographers independently reviewed original sonographic images of each nodule and classified it using the 2015 American Thyroid Association (ATA) guidelines and the Thyroid Imaging Reporting and Data System (TI-RADS) classification proposed by Korean radiologists; later, images were reviewed jointly to obtain consensus classifications of each nodule. Original cytology slides were similarly reviewed by three experienced cytopathologists, who reclassified the nodule (independently, then jointly) according to revised Italian Consensus on Thyroid Cytology (ICTC-2014) criteria. Consensus ICTC-2014, ATA, and TI-RADS classifications were analyzed against surgical histology reports to estimate each system’s sensitivity, specificity, positive and negative predictive values.

Results

Of the 49 indeterminate nodules examined, 30 (61.2 %) were histologically benign. Consensus ICTC-2014 classification correctly classified malignant nodules with positive predictive value of 50 % and negative predictive value of 90 %. Sonographic classification of nodules as intermediate to high suspicion by ATA or TI-RADS category 4c displayed positive predictive value of 63 and 71 %, respectively; positive predictive values dropped to 44 and 42 % when lower positivity thresholds were used (ATA low suspicion, TI-RADS category 4a). Negative predictive values for ATA and TI-RADS were 91 and 74 %, respectively, with higher positivity thresholds and 100 % for both with lower thresholds. All systems displayed appreciable inter-observer variability (Krippendorff alphas: ATA 0.36, TIRADS 0.42, ICTC-2014 0.74).

Conclusions

With stringent negativity cut-offs, American Thyroid Association and Thyroid Imaging Reporting and Data System assessment of cytologically indeterminate thyroid nodules allows high-confidence exclusion of malignancy.

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References

  1. H. Gharib, E. Papini, R. Paschke, D.S. Duick, R. Valcavi, L. Hegedüs, P. Vitti, American Association of Clinical Endocrinologists, Associazione Medici Endocrinologi, and European Thyroid Association medical guidelines for clinical practice for the diagnosis and management of thyroid nodules. Endocr. Pr. 16(Suppl 1),1–43 (2010)

    Google Scholar 

  2. British Thyroid Association and Royal College of Physicians. Guidelines for the Management of Thyroid Cancer in Adults. (RCP, London), 2002)

    Google Scholar 

  3. G. Fadda, F. Basolo, A. Bondi, G. Bussolati, A. Crescenzi, O. Nappi, F. Nardi, M. Papotti, G. Taddei, L. Palombini, Cytological classification of thyroid nodules. Proposal of the SIAPEC-IAP Italian consensus working group. Pathologica 102, 405–408 (2010)

    CAS  PubMed  Google Scholar 

  4. E.S. Cibas, S.Z. Ali, The bethesda system for reporting thyroid cytopathology. Am. J. Clin. Pathol. 132, 658–665 (2009)

    Article  PubMed  Google Scholar 

  5. F. Nardi, F. Basolo, A. Crescenzi, G. Fadda, A. Frasoldati, F. Orlandi, L. Palombini, E. Papini, M. Zini, A. Pontecorvi, P. Vitti, Italian consensus for the classification and reporting of thyroid cytology. J. Endocrinol. Invest. 37, 593–599 (2014)

    Article  PubMed  Google Scholar 

  6. 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, 1253–1263 (2014)

    Article  CAS  PubMed  Google Scholar 

  7. H.K. Su, L.L. Dos Reis, M.A. Lupo, M. Milas, L.A. Orloff, J.E. Langer, E.M. Brett, E. Kazam, S.L. Lee, G. Minkowitz, E.H. Alpert, E.H. Dewey, M.L. Urken, Striving toward standardization of reporting of ultrasound features of thyroid nodules and lymph nodes: a multidisciplinary consensus statement. Thyroid 24, 1341–1349 (2014)

    Article  PubMed  Google Scholar 

  8. J.Y. Kwak, K.H. Han, J.H. Yoon, H.J. Moon, E.J. Son, S.H. Park, H.K. Jung, J.S. Choi, B.M. Kim, E.K. Kim, Thyroid imaging reporting and data system for US features of nodules: a step in establishing better stratification of cancer risk. Radiology 260, 892–899 (2011)

    Article  PubMed  Google Scholar 

  9. 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, 1–133 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  10. M.J. Kim, E.K. Kim, S.I. Park, B.M. Kim, J.Y. Kwak, S.J. Kim, J.H. Youk, S.H. Park, US-guided fine-needle aspiration of thyroid nodules: indications, techniques, results. Radiographics 28, 1869–1886 (2008). discussion 1887

    Article  PubMed  Google Scholar 

  11. E.G. Grant, F.N. Tessler, J.K. Hoang, J.E. Langer, M.D. Beland, L.L. Berland, J.J. Cronan, T.S. Desser, M.C. Frates, U.M. Hamper, W.D. Middleton, C.C. Reading, L.M. Scoutt, A.T. Stavros, S.A. Teefey, Thyroid ultrasound reporting lexicon: white paper of the ACR thyroid imaging, reporting and data system (TIRADS) committee. J. Am. Coll. Radiol. JACR 12, 1272–1279 (2015)

    Article  PubMed  Google Scholar 

  12. A.F. Hayes, K. Krippendorff, Answering the call for a standard reliability measure for coding data. Commun. Methods Meas 1, 77–89 (2007)

    Article  Google Scholar 

  13. B.R. Englum, J. Pura, S.D. Reed, S.A. Roman, J.A. Sosa, R.P. Scheri, A bedside risk calculator to preoperatively distinguish follicular thyroid carcinoma from follicular variant of papillary thyroid Carcinoma. World J. Surg. 39, 2928–2934 (2015)

    Article  PubMed  Google Scholar 

  14. B. Aschebrook-Kilfoy, R.H. Grogan, M.H. Ward, E. Kaplan, S.S. Devesa, Follicular thyroid cancer incidence patterns in the United States, 1980-2009. Thyroid 23, 1015–1021 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  15. Y. Tutuncu, D. Berker, S. Isik, G. Akbaba, U. Ozuguz, F.K. Kucukler, E. Göcmen, Y. Yalcın, Y. Aydin, S. Guler, The frequency of malignancy and the relationship between malignancy and ultrasonographic features of thyroid nodules with indeterminate cytology. Endocrine 45, 37–45 (2014)

    Article  CAS  PubMed  Google Scholar 

  16. F. Ianni, P. Campanella, C.A. Rota, A. Prete, L. Castellino, A. Pontecorvi, S.M. Corsello, A meta-analysis-derived proposal for a clinical, ultrasonographic, and cytological scoring system to evaluate thyroid nodules: the “CUT” score. Endocrine 52, 313–321 (2016)

    Article  CAS  PubMed  Google Scholar 

  17. F. Garino, M. Deandrea, M. Motta, A. Mormile, F. Ragazzoni, N. Palestini, M. Freddi, G. Gasparri, E. Sgotto, D. Pacchioni, P.P. Limone, Diagnostic performance of elastography in cytologically indeterminate thyroid nodules. Endocrine 49, 175–183 (2015)

    Article  CAS  PubMed  Google Scholar 

  18. P. Trimboli, G. Treglia, R. Sadeghi, F. Romanelli, L. Giovanella, Reliability of real-time elastography to diagnose thyroid nodules previously read at FNAC as indeterminate: a meta-analysis. Endocrine 50, 335–343 (2015)

    Article  CAS  PubMed  Google Scholar 

  19. N. Nasrollah, P. Trimboli, L. Guidobaldi, D.D. Cicciarella Modica, C. Ventura, G. Ramacciato, S. Taccogna, F. Romanelli, S. Valabrega, A. Crescenzi, Thin core biopsy should help to discriminate thyroid nodules cytologically classified as indeterminate. A new sampling technique. Endocrine 43, 659–665 (2013)

    Article  CAS  PubMed  Google Scholar 

  20. C.L. Chng, T.R. Kurzawinski, T. Beale, Value of sonographic features in predicting malignancy in thyroid nodules diagnosed as follicular neoplasm on cytology. Clin. Endocrinol. Oxf. 83, 711–716 (2015)

    Article  PubMed  Google Scholar 

  21. S.H. Choi, E.K. Kim, J.Y. Kwak, M.J. Kim, E.J. Son, Interobserver and intraobserver variations in ultrasound assessment of thyroid nodules. Thyroid 20, 167–172 (2010)

    Article  PubMed  Google Scholar 

  22. C.S. Park, S.H. Kim, S.L. Jung, B.J. Kang, J.Y. Kim, J.J. Choi, M.S. Sung, H.W. Yim, S.H. Jeong, Observer variability in the sonographic evaluation of thyroid nodules. J. Clin. Ultrasound 38, 287–293 (2010)

    PubMed  Google Scholar 

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Acknowledgments

Medical writing was provided by M.E. Kent (EMWA) and funded by the Fondazione Umberto Di Mario. GG and LL contributed to this paper as recipients of the PhD program of Biotechnologies and Clinical Medicine of the University of Rome, Sapienza.

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Correspondence to Cosimo Durante.

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Grani, G., Lamartina, L., Ascoli, V. et al. Ultrasonography scoring systems can rule out malignancy in cytologically indeterminate thyroid nodules. Endocrine 57, 256–261 (2017). https://doi.org/10.1007/s12020-016-1148-6

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