Performance of a dual-component molecular assay in cytologically indeterminate thyroid nodules

Endocrine - Tập 68 Số 2 - Trang 458-465 - 2020
Marialuisa Sponziello1, Chiara Brunelli2, Antonella Verrienti1, Giorgio Grani1, Valeria Pecce1, Luana Abballe1, Valeria Ramundo1, Giuseppe Damante3, Diego Russo4, Celestino Pio Lombardi5, Cosimo Durante1, Esther Diana Rossi2, Patrizia Straccia2, Guido Fadda2, Sébastiano Filetti1
1Department of translational and precision medicine, “Sapienza” University of Rome, 00161, Rome, Italy
2Division of Anatomic Pathology and Histology Catholic University of Sacred Heart, Foundation “Agostino Gemelli” University Hospital, Rome, Italy
3Department of Medicine, University of Udine, 33100, Udine, Italy
4Department of Health Sciences, “Magna Graecia” University of Catanzaro, 88100, Catanzaro, Italy
5Division of Endocrine Surgery, Catholic University of Sacred Heart, Foundation “Agostino Gemelli” University Hospital, Rome, Italy

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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). https://doi.org/10.1089/thy.2015.0020

C. Durante, G. Grani, L. Lamartina, S. Filetti, S.J. Mandel, D.S. Cooper, The diagnosis and management of thyroid nodules: a review. JAMA 319, 914–924 (2018). https://doi.org/10.1001/jama.2018.0898

M. Bongiovanni, A. Spitale, W.C. Faquin, L. Mazzucchelli, Z.W. Baloch, The Bethesda system for reporting thyroid cytopathology: a meta-analysis. Acta Cytol. 56, 333–339 (2012). https://doi.org/10.1159/000339959

E.S. Cibas, S.Z. Ali, The 2017 Bethesda system for reporting thyroid cytopathology. J. Am. Soc. Cytopathol. 6, 217–222 (2017). https://doi.org/10.1016/j.jasc.2017.09.002

Z.W. Baloch, V.A. LiVolsi, S.L. Asa, J. Rosai, M.J. Merino, G. Randolph, P. Vielh, R.M. DeMay, M.K. Sidawy, W.J. Frable, Diagnostic terminology and morphologic criteria for cytologic diagnosis of thyroid lesions: a synopsis of the national cancer institute thyroid fine-needle aspiration state of the science conference. Diagn. Cytopathol. 36, 425–437 (2008). https://doi.org/10.1002/dc.20830

N. Agrawal, R. Akbani, B.A. Aksoy, A. Ally, H. Arachchi, S.L. Asa, J.T. Auman, M. Balasundaram, S. Balu, S.B. Baylin, M. Behera, B. Bernard, R. Beroukhim, J.A. Bishop, A.D. Black, T. Bodenheimer, L. Boice, M.S. Bootwalla, J. Bowen, R. Bowlby, C.A. Bristow, R. Brookens, D. Brooks, R. Bryant, E. Buda, Y.S.N. Butterfield, T. Carling, R. Carlsen, S.L. Carter, S.E. Carty, T.A. Chan, A.Y. Chen, A.D. Cherniack, D. Cheung, L. Chin, J. Cho, A. Chu, E. Chuah, K. Cibulskis, G. Ciriello, A. Clarke, G.L. Clayman, L. Cope, J.A. Copland, K. Covington, L. Danilova, T. Davidsen, J.A. Demchok, D. DiCara, N. Dhalla, R. Dhir, S.S. Dookran, G. Dresdner, J. Eldridge, G. Eley, A.K. El-Naggar, S. Eng, J.A. Fagin, T. Fennell, R.L. Ferris, S. Fisher, S. Frazer, J. Frick, S.B. Gabriel, I. Ganly, J. Gao, L.A. Garraway, J.M. Gastier-Foster, G. Getz, N. Gehlenborg, R. Ghossein, R.A. Gibbs, T.J. Giordano, K. Gomez-Hernandez, J. Grimsby, B. Gross, R. Guin, A. Hadjipanayis, H.A. Harper, D.N. Hayes, D.I. Heiman, J.G. Herman, K.A. Hoadley, M. Hofree, R.A. Holt, A.P. Hoyle, F.W. Huang, M. Huang, C.M. Hutter, T. Ideker, L. Iype, A. Jacobsen, S.R. Jefferys, C.D. Jones, S.J.M. Jones, K. Kasaian, E. Kebebew, F.R. Khuri, J. Kim, R. Kramer, R. Kreisberg, R. Kucherlapati, D.J. Kwiatkowski, M. Ladanyi, P.H. Lai, P.W. Laird, E. Lander, M.S. Lawrence, D. Lee, E. Lee, S. Lee, W. Lee, K.M. Leraas, T.M. Lichtenberg, L. Lichtenstein, P. Lin, S. Ling, J. Liu, W. Liu, Y. Liu, V.A. LiVolsi, Y. Lu, Y. Ma, H.S. Mahadeshwar, M.A. Marra, M. Mayo, D.G. McFadden, S. Meng, M. Meyerson, P.A. Mieczkowski, M. Miller, G. Mills, R.A. Hadjipanayis, L.E. Mose, A.J. Mungall, B.A. Murray, Y.E. Nikiforov, M.S. Noble, A.I. Ojesina, T.K. Owonikoko, B.A. Ozenberger, A. Pantazi, M. Parfenov, P.J. Park, J.S. Parker, E.O. Paull, C.S. Pedamallu, C.M. Perou, J.F. Prins, A. Protopopov, S.S. Ramalingam, N.C. Ramirez, R. Ramirez, B.J. Raphael, W.K. Rathmell, X. Ren, S.M. Reynolds, E. Rheinbay, M.D. Ringel, M. Rivera, J. Roach, A.G. Robertson, M.W. Rosenberg, M. Rosenthal, S. Sadeghi, G. Saksena, C. Sander, N. Santoso, J.E. Schein, N. Schultz, S.E. Schumacher, R.R. Seethala, J. Seidman, Y. Senbabaoglu, S. Seth, S. Sharpe, K.R.M. Shaw, J.P. Shen, R. Shen, S. Sherman, M. Sheth, Y. Shi, I. Shmulevich, G.L. Sica, J.V. Simons, R. Sinha, P. Sipahimalani, R.C. Smallridge, H.J. Sofia, M.G. Soloway, X. Song, C. Sougnez, C. Stewart, P. Stojanov, J.M. Stuart, S.O. Sumer, Y. Sun, B. Tabak, A. Tam, D. Tan, J. Tang, R. Tarnuzzer, B.S. Taylor, N. Thiessen, L. Thorne, V. Thorsson, R.M. Tuttle, C.B. Umbricht, D.J. Van Den Berg, F. Vandin, U. Veluvolu, R.G.W. Verhaak, M. Vinco, D. Voet, V. Walter, Z. Wang, S. Waring, P.M. Weinberger, N. Weinhold, J.N. Weinstein, D.J. Weisenberger, D. Wheeler, M.D. Wilkerson, J. Wilson, M. Williams, D.A. Winer, L. Wise, J. Wu, L. Xi, A.W. Xu, L. Yang, L. Yang, T.I. Zack, M.A. Zeiger, D. Zeng, J.C. Zenklusen, N. Zhao, H. Zhang, J. Zhang, J.(Julia) Zhang, W. Zhang, E. Zmuda, L. Zou, Integrated genomic characterization of papillary thyroid carcinoma. Cell 159, 676–690 (2015). https://doi.org/10.1016/j.cell.2014.09.050

I. Landa, T. Ibrahimpasic, L. Boucai, R. Sinha, J.A. Knauf, R.H. Shah, S. Dogan, J.C. Ricarte-Filho, G.P. Krishnamoorthy, B. Xu, N. Schultz, M.F. Berger, C. Sander, B.S. Taylor, R. Ghossein, I. Ganly, J.A. Fagin, Genomic and transcriptomic hallmarks of poorly-differentiated and anaplastic thyroid cancers. J. Clin. Invest. 126, 1052–1066 (2016). https://doi.org/10.1172/JCI85271

C. Ferraz, Can current molecular tests help in the diagnosis of indeterminate thyroid nodule FNAB? Arch. Endocrinol. Metab. 62, 576–584 (2018). https://doi.org/10.20945/2359-3997000000081

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). https://doi.org/10.1007/s40618-014-0062-0

E.S. Cibas, S.Z. Ali, The 2017 Bethesda system for reporting thyroid cytopathology. J. Am. Soc. Cytopathol. 6, 217–222 (2017). https://doi.org/10.1016/j.jasc.2017.09.002

M. Sponziello, S. Benvenuti, A. Gentile, V. Pecce, F. Rosignolo, A.R. Virzì, M. Milan, P.M. Comoglio, E. Londin, P. Fortina, A. Barnabei, M. Appetecchia, F. Marandino, D. Russo, S. Filetti, C. Durante, A. Verrienti, Whole exome sequencing identifies a germline MET mutation in two siblings with hereditary wild-type RET medullary thyroid cancer. Hum. Mutat. 39, 371–377 (2018). https://doi.org/10.1002/humu.23378

M. Sponziello, G. Silvestri, A. Verrienti, A. Perna, F. Rosignolo, C. Brunelli, V. Pecce, E.D. Rossi, C.P. Lombardi, C. Durante, S. Filetti, G. Fadda, A novel nonsense EIF1AX mutation identified in a thyroid nodule histologically diagnosed as oncocytic carcinoma. Endocrine 62, 492–495 (2018)

L.M. Mulligan, Exploiting insights on the RET receptor for personalized cancer medicine. Endocr. Relat. Cancer. 25, T189–T200 (2018). https://doi.org/10.1530/ERC-18-0141

Y.E. Nikiforov, Role of molecular markers in thyroid nodule management: then and now. Endocr. Pract. 23, 979–988 (2017). https://doi.org/10.4158/EP171805.RA

F. Rosignolo, L. Memeo, F. Monzani, C. Colarossi, V. Pecce, A. Verrienti, C. Durante, G. Grani, L. Lamartina, S. Forte, D. Martinetti, D. Giuffrida, D. Russo, F. Basolo, S. Filetti, M. Sponziello, MicroRNA-based molecular classification of papillary thyroid carcinoma. Int. J. Oncol. 50, 1767–1777 (2017). https://doi.org/10.3892/ijo.2017.3960

F. Rosignolo, M. Sponziello, L. Giacomelli, D. Russo, V. Pecce, M. Biffoni, R. Bellantone, C.P. Lombardi, L. Lamartina, G. Grani, C. Durante, S. Filetti, A. Verrienti, Identification of Thyroid-Associated Serum microRNA Profiles and Their Potential Use in Thyroid Cancer Follow-Up. J. Endocr. Soc. 1, 3–13 (2017). https://doi.org/10.1210/js.2016-1032

M. Celano, F. Rosignolo, V. Maggisano, V. Pecce, M. Iannone, D. Russo, S. Bulotta, MicroRNAs as biomarkers in thyroid carcinoma. Int. J. Genomics 2017, 6496570 (2017). https://doi.org/10.1155/2017/6496570

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, 256–261 (2017). https://doi.org/10.1007/s12020-016-1148-6

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, 1004–1012 (2018). https://doi.org/10.1089/thy.2018.0085

T. Rago, M. Scutari, F. Santini, V. Loiacono, P. Piaggi, G. Di Coscio, F. Basolo, P. Berti, A. Pinchera, P. Vitti, Real-time elastosonography: useful tool for refining the presurgical diagnosis in thyroid nodules with indeterminate or nondiagnostic cytology. J. Clin. Endocrinol. Metab. 95, 5274–5280 (2010). https://doi.org/10.1210/jc.2010-0901

V. Cantisani, E. David, H. Grazhdani, A. Rubini, M. Radzina, C.F. Dietrich, C. Durante, L. Lamartina, G. Grani, A. Valeria, D. Bosco, C. Di Gioia, F.M. Frattaroli, V. D’Andrea, C. De Vito, D. Fresilli, F. D’Ambrosio, L. Giacomelli, C. Catalano, Prospective evaluation of semiquantitative strain ratio and quantitative 2D ultrasound shear wave elastography (SWE) in association with TIRADS classification for thyroid nodule characterization. Ultraschall Med. 40, 495–503 (2019). https://doi.org/10.1055/a-0853-1821

F. Ianni, D. Pascucci, R.M. Paragliola, C.A. Rota, G. Perotti, G. Fadda, A. Pontecorvi, S.M. Corsello, Follow-up or surgery for indeterminate thyroid nodules: could the CUT score application be a support for decision making in the preoperative assessment? Thyroid 30, 65–71 (2019). https://doi.org/10.1089/thy.2018.0649

Z.W. Baloch, S. Fleisher, V.A. LiVolsi, P.K. Gupta, Diagnosis of follicular neoplasm: a gray zone in thyroid fine-needle aspiration cytology. Diagn. Cytopathol. 26, 41–44 (2002). https://doi.org/10.1002/dc.10043

R. Promberger, J. Ott, F. Kober, M. Karik, M. Freissmuth, M. Hermann, Normal parathyroid hormone levels do not exclude permanent hypoparathyroidism after thyroidectomy. Thyroid 21, 145–150 (2011). https://doi.org/10.1089/thy.2010.0067

E. Kandil, B. Krishnan, S.I. Noureldine, L. Yao, R.P. Tufano, Hemithyroidectomy: a meta-analysis of postoperative need for hormone replacement and complications. ORL 75, 6–17 (2013). https://doi.org/10.1159/000345498

J.A. Sosa, H.M. Bowman, J.M. Tielsch, N.R. Powe, T.A. Gordon, R. Udelsman, The importance of surgeon experience for clinical and economic outcomes from thyroidectomy. Ann. Surg. 228, 320–330 (1998). https://doi.org/10.1097/00000658-199809000-00005

H. Verloop, M. Louwerens, J.W. Schoones, J. Kievit, J.W.A. Smit, O.M. Dekkers, Risk of hypothyroidism following hemithyroidectomy: systematic review and meta-analysis of prognostic studies. J. Clin. Endocrinol. Metab. 97, 2243–2255 (2012). https://doi.org/10.1210/jc.2012-1063

S. Filetti, P.W. Ladenson, M. Biffoni, M.G. D’Ambrosio, L. Giacomelli, S. Lopatriello, The true cost of thyroid surgery determined by a micro-costing approach. Endocrine 55, 519–529 (2017). https://doi.org/10.1007/s12020-016-0980-z

K.N. Patel, T.E. Angell, J. Babiarz, N.M. Barth, T. Blevins, Q.-Y. Duh, R.A. Ghossein, R.M. Harrell, J. Huang, G.C. Kennedy, S.Y. Kim, R.T. Kloos, V.A. LiVolsi, G.W. Randolph, P.M. Sadow, M.H. Shanik, J.A. Sosa, S.T. Traweek, P.S. Walsh, D. Whitney, M.W. Yeh, P.W. Ladenson, Performance of a genomic sequencing classifier for the preoperative diagnosis of cytologically indeterminate thyroid nodules. JAMA Surg. 153, 817–824 (2018). https://doi.org/10.1001/jamasurg.2018.1153

Y.E. Nikiforov, D.L. Steward, S.E. Carty, R.S. Sippel, S.P. Yang, J.A. Sosa, J.A. Sipos, J.J. Figge, S. Mandel, B.R. Haugen, K.D. Burman, Z.W. Baloch, R.V. Lloyd, R.R. Seethala, W.E. Gooding, S.I. Chiosea, C. Gomes-Lima, R.L. Ferris, J.M. Folek, R.A. Khawaja, P. Kundra, K.S. Loh, C.B. Marshall, S. Mayson, K.L. McCoy, M.E. Nga, K.Y. Ngiam, M.N. Nikiforova, J.L. Poehls, M.D. Ringel, H. Yang, L. Yip, Performance of a multigene genomic classifier in thyroid nodules with indeterminate cytology: a prospective blinded multicenter study. JAMA Oncol. 5, 204–212 (2019). https://doi.org/10.1001/jamaoncol.2018.4616

M.N. Nikiforova, S. Mercurio, A.I. Wald, M. Barbi de Moura, K. Callenberg, L. Santana-Santos, W.E. Gooding, L. Yip, R.L. Ferris, Y.E Nikiforov, Analytical performance of the ThyroSeq v3 genomic classifier for cancer diagnosis in thyroid nodules. Cancer 124, 1682–1690 (2018). https://doi.org/10.1002/cncr.31245

E. Labourier, A. Shifrin, A.E. Busseniers, M.A. Lupo, M.L. Manganelli, B. Andruss, D. Wylie, S. Beaudenon-Huibregtse, Molecular testing for miRNA, mRNA, and DNA on fine-needle aspiration improves the preoperative diagnosis of thyroid nodules with indeterminate cytology. J. Clin. Endocrinol. Metab. 100, 2743–2750 (2015). https://doi.org/10.1210/jc.2015-1158

A.B. Banizs, J.F. Silverman, The utility of combined mutation analysis and microRNA classification in reclassifying cancer risk of cytologically indeterminate thyroid nodules. Diagn. Cytopathol. 47, 268–274 (2019). https://doi.org/10.1002/dc.24087

G. Lithwick-Yanai, N. Dromi, A. Shtabsky, S. Morgenstern, Y. Strenov, M. Feinmesser, V. Kravtsov, M.E. Leon, M. Hajdúch, S.Z. Ali, C.J. VandenBussche, X. Zhang, L. Leider-Trejo, A. Zubkov, S. Vorobyov, M. Kushnir, Y. Goren, S. Tabak, E. Kadosh, H. Benjamin, T. Schnitzer-Perlman, H. Marmor, M. Motin, D. Lebanony, S. Kredo-Russo, H. Mitchell, M. Noller, A. Smith, O. Dattner, K. Ashkenazi, M. Sanden, K.A. Berlin, D. Bar, E. Meiri, Multicentre validation of a microRNA-based assay for diagnosing indeterminate thyroid nodules utilising fine needle aspirate smears. J. Clin. Pathol. 70, 500–507 (2017). https://doi.org/10.1136/jclinpath-2016-204089