Skip to main content
Top
Published in: Endocrine 2/2017

01-08-2017 | Original Article

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

Authors: Giorgio Grani, Livia Lamartina, Valeria Ascoli, Daniela Bosco, Francesco Nardi, Ferdinando D’Ambrosio, Antonello Rubini, Laura Giacomelli, Marco Biffoni, Sebastiano Filetti, Cosimo Durante, Vito Cantisani

Published in: Endocrine | Issue 2/2017

Login to get access

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.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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) 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)
2.
go back to reference British Thyroid Association and Royal College of Physicians. Guidelines for the Management of Thyroid Cancer in Adults. (RCP, London), 2002) British Thyroid Association and Royal College of Physicians. Guidelines for the Management of Thyroid Cancer in Adults. (RCP, London), 2002)
3.
go back to reference 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)PubMed 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)PubMed
4.
go back to reference E.S. Cibas, S.Z. Ali, The bethesda system for reporting thyroid cytopathology. Am. J. Clin. Pathol. 132, 658–665 (2009)CrossRefPubMed E.S. Cibas, S.Z. Ali, The bethesda system for reporting thyroid cytopathology. Am. J. Clin. Pathol. 132, 658–665 (2009)CrossRefPubMed
5.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
6.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
7.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
8.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
9.
go back to reference 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)CrossRefPubMedPubMedCentral 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)CrossRefPubMedPubMedCentral
10.
go back to reference 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 1887CrossRefPubMed 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 1887CrossRefPubMed
11.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
12.
go back to reference A.F. Hayes, K. Krippendorff, Answering the call for a standard reliability measure for coding data. Commun. Methods Meas 1, 77–89 (2007)CrossRef A.F. Hayes, K. Krippendorff, Answering the call for a standard reliability measure for coding data. Commun. Methods Meas 1, 77–89 (2007)CrossRef
13.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
14.
go back to reference 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)CrossRefPubMedPubMedCentral 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)CrossRefPubMedPubMedCentral
15.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
16.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
17.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
18.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
19.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
20.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
21.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
22.
go back to reference 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 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
Metadata
Title
Ultrasonography scoring systems can rule out malignancy in cytologically indeterminate thyroid nodules
Authors
Giorgio Grani
Livia Lamartina
Valeria Ascoli
Daniela Bosco
Francesco Nardi
Ferdinando D’Ambrosio
Antonello Rubini
Laura Giacomelli
Marco Biffoni
Sebastiano Filetti
Cosimo Durante
Vito Cantisani
Publication date
01-08-2017
Publisher
Springer US
Published in
Endocrine / Issue 2/2017
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-016-1148-6

Other articles of this Issue 2/2017

Endocrine 2/2017 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.