Ruling in or ruling out thyroid malignancy by molecular diagnostics of thyroid nodules

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 28, Issue 4, 2014, Pages 545-557

  Eszlinger, Markus ^a   Hegedüs, László ^b   Paschke, Ralf ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

cytology; fine needle aspiration; molecular diagnostics; thyroid cancer

Indexed keywords

MICRORNA;

BRAF GENE; CYTOLOGY; FINE NEEDLE ASPIRATION BIOPSY; GENE; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; HRAS GENE; HUMAN; INTERMETHOD COMPARISON; KRAS GENE; MOLECULAR DIAGNOSTICS; NRAS GENE; PAX8 GENE; POINT MUTATION; PREDICTIVE VALUE; RET GENE; REVIEW; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS; SOMATIC MUTATION; THYROID CANCER; THYROID NODULE; DIFFERENTIAL DIAGNOSIS; GENETICS; GOITER, NODULAR; HIGH THROUGHPUT SEQUENCING; MOLECULAR DIAGNOSIS; MUTATION; PATHOLOGY; PROCEDURES;

BIOPSY, FINE-NEEDLE; DIAGNOSIS, DIFFERENTIAL; GOITER, NODULAR; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MOLECULAR DIAGNOSTIC TECHNIQUES; MUTATION; THYROID NODULE;

EID: 84904754772     PISSN: 1521690X     EISSN: 15321908     Source Type: Journal    
DOI: 10.1016/j.beem.2014.01.011     Document Type: Review

References (91)

1. British Thyroid Association and Royal College of Physicians Guidelines for the management of thyroid cancer 2 ed. 2007 RCP London
2. H. Gharib, E. Papini, and R. Paschke et al. American association of clinical endocrinologists, Italian association of clinical endocrinologists and European thyroid association medical guidelines for clinical practice for the diagnosis and management of thyroid nodules Endocr Pract 16 Suppl. 1 2010 1 43
3. M. Eszlinger, and R. Paschke Molecular fine-needle aspiration biopsy diagnosis of thyroid nodules by tumor specific mutations and gene expression patterns Mol Cell Endocrinol 322 1-2 2010 29 37
4. L. Hegedus Clinical practice. The thyroid nodule N Engl J Med 351 17 2004 1764 1771
5. R. Paschke, L. Hegedus, and E. Alexander et al. Thyroid nodule guidelines: agreement, disagreement and need for future research Nat Rev Endocrinol 7 6 2011 354 361
6. R. Camargo, S. Corigliano, and C. Friguglietti et al. Latin American thyroid society recommendations for the management of thyroid nodules Arq Bras Endocrinol Metabol 53 9 2009 1167 1175
7. D.S. Cooper, G.M. Doherty, and B.R. Haugen et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer Thyroid 19 11 2009 1167 1214
8. E.S. Cibas, Z.W. Baloch, and G. Fellegara et al. A prospective assessment defining the limitations of thyroid nodule pathologic evaluation Ann Intern Med 159 5 2013 325 332
9. M. Xing Molecular pathogenesis and mechanisms of thyroid cancer Nat Rev Cancer 13 3 2013 184 199
10. C. Ferraz, M. Eszlinger, and R. Paschke Current state and future perspective of molecular diagnosis of fine-needle aspiration biopsy of thyroid nodules J Clin Endocrinol Metab 96 7 2011 2016 2026
11. C. Ferraz, C. Rehfeld, and A. Krogdahl et al. Detection of PAX8/PPARG and RET/PTC rearrangements is feasible in routine air-dried Fine needle aspiration smears Thyroid 22 10 2012 1025 1030
12. S. Cantara, M. Capezzone, and S. Marchisotta et al. Impact of proto-oncogene mutation detection in cytological specimens from thyroid nodules improves the diagnostic accuracy of cytology J Clin Endocrinol Metab 95 3 2010 1365 1369
13. W. Moses, J. Weng, and I. Sansano et al. Molecular testing for somatic mutations improves the accuracy of thyroid fine-needle aspiration biopsy World J Surg 34 11 2010 2589 2594
14. Y.E. Nikiforov, D.L. Steward, and T.M. Robinson-Smith et al. Molecular testing for mutations in improving the Fine needle aspiration diagnosis of thyroid nodules J Clin Endocrinol Metab 94 6 2009 2092 2098
15. Y.E. Nikiforov, N.P. Ohori, and S.P. Hodak et al. Impact of mutational testing on the diagnosis and management of patients with cytologically indeterminate thyroid nodules: a prospective analysis of 1056 FNA samples J Clin Endocrinol Metab 96 11 2011 3390 3397
16. N.P. Ohori, M.N. Nikiforova, and K.E. Schoedel et al. Contribution of molecular testing to thyroid fine-needle aspiration cytology of "follicular lesion of undetermined significance/atypia of undetermined significance" Cancer Cytopathol 118 1 2010 17 23
17. L. Rosato, N. Avenia, and P. Bernante et al. Complications of thyroid surgery: analysis of a multicentric study on 14,934 patients operated on in Italy over 5 years World J Surg 28 3 2004 271 276
18. D.S. Cooper, G.M. Doherty, and B.R. Haugen et al. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer Thyroid 16 2 2006 109 142
19. Y. Cohen, E. Rosenbaum, and D.P. Clark et al. Mutational analysis of BRAF in fine needle aspiration biopsies of the thyroid: a potential application for the preoperative assessment of thyroid nodules Clin Cancer Res 10 8 2004 2761 2765
20. S. Girlando, L.V. Cuorvo, and M. Bonzanini et al. High prevalence of B-RAF mutation in papillary carcinoma of the thyroid in north-east Italy Int J Surg Pathol 18 3 2010 173 176
21. S.Y. Nam, B.K. Han, and E.Y. Ko et al. BRAF V600E mutation analysis of thyroid nodules needle aspirates in relation to their ultrasongraphic classification: a potential guide for selection of samples for molecular analysis Thyroid 20 3 2010 273 279
22. G. Pizzolanti, L. Russo, and P. Richiusa et al. Fine-Needle aspiration molecular analysis for the diagnosis of papillary thyroid carcinoma through BRAF(V600E) mutation and RET/PTC rearrangement Thyroid 17 11 2007 1109 1115
23. M.C. Zatelli, G. Trasforini, and S. Leoni et al. BRAF V600E mutation analysis increases diagnostic accuracy for papillary thyroid carcinoma in fine-needle aspiration biopsies Eur J Endocrinol 161 3 2009 467 473
24. Y.E. Nikiforov, and M.N. Nikiforova Molecular genetics and diagnosis of thyroid cancer Nat Rev Endocrinol 7 10 2011 569 580
25. Z.W. Baloch, E.S. Cibas, and D.P. Clark et al. The national cancer institute thyroid fine needle aspiration state of the science conference: a summation Cytojournal 5 2008 6
26. C. Rehfeld, S. Munz, and A. Krogdahl et al. Impact of different methodologies on the detection of Point mutations in routine air-dried Fine needle aspiration (FNA) smears Horm Metab Res 45 7 2013 513 517
27. M. Eszlinger, A. Krogdahl, and S. Munz et al. Impact of molecular screening for Point mutations and rearrangements in routine air-dried Fine-Needle aspiration samples of thyroid nodules Thyroid 2013 [Epub ahead of print], PMID: 23837487
28. A. Guerra, M.R. Sapio, and V. Marotta et al. The primary occurrence of BRAF(V600E) is a rare clonal event in papillary thyroid carcinoma J Clin Endocrinol Metab 97 2 2012 517 524
29. K. Unger, H. Zitzelsberger, and G. Salvatore et al. Heterogeneity in the distribution of RET/PTC rearrangements within individual post-Chernobyl papillary thyroid carcinomas J Clin Endocrinol Metab 89 9 2004 4272 4279
30. Z. Zhu, R. Ciampi, and M.N. Nikiforova et al. Prevalence of RET/PTC rearrangements in thyroid papillary carcinomas: effects of the detection methods and genetic heterogeneity J Clin Endocrinol Metab 91 9 2006 3603 3610
31. N. Gupta, A.K. Dasyam, and S.E. Carty et al. RAS mutations in thyroid FNA specimens are highly predictive of predominantly low-risk follicular-pattern cancers J Clin Endocrinol Metab 98 5 2013 E914 E922
32. F. Basolo, F. Pisaturo, and L.E. Pollina et al. N-ras mutation in poorly differentiated thyroid carcinomas: correlation with bone metastases and inverse correlation to thyroglobulin expression Thyroid 10 1 2000 19 23
33. M. Fukahori, A. Yoshida, and H. Hayashi et al. The associations between RAS mutations and clinical characteristics in follicular thyroid tumors: new insights from a single center and a large patient cohort Thyroid 22 7 2012 683 689
34. G. Garcia-Rostan, H. Zhao, and R.L. Camp et al. ras mutations are associated with aggressive tumor phenotypes and poor prognosis in thyroid cancer J Clin Oncol 21 17 2003 3226 3235
35. Z. Zhu, M. Gandhi, and M.N. Nikiforova et al. Molecular profile and clinical-pathologic features of the follicular variant of papillary thyroid carcinoma. An unusually high prevalence of ras mutations Am J Clin Pathol 120 1 2003 71 77
36. J.A. Fagin Minireview: branded from the start-distinct oncogenic initiating events may determine tumor fate in the thyroid Mol Endocrinol 16 5 2002 903 911
37. H.I. Saavedra, J.A. Knauf, and J.M. Shirokawa et al. The RAS oncogene induces genomic instability in thyroid PCCL3 cells via the MAPK pathway Oncogene 19 34 2000 3948 3954
38. S.C. Kamran, E. Marqusee, and M.I. Kim et al. Thyroid nodule size and prediction of cancer J Clin Endocrinol Metab 98 2 2013 564 570
39. C.S. Kim, and X. Zhu Lessons from mouse models of thyroid cancer Thyroid 19 12 2009 1317 1331
40. P. Rochefort, B. Caillou, and F.M. Michiels et al. Thyroid pathologies in transgenic mice expressing a human activated Ras gene driven by a thyroglobulin promoter Oncogene 12 1 1996 111 118
41. M.R. Sapio, A. Guerra, and V. Marotta et al. High growth rate of benign thyroid nodules bearing RET/PTC rearrangements J Clin Endocrinol Metab 96 6 2011 E916 E919
42. M. Xing, D. Clark, and H. Guan et al. BRAF mutation testing of thyroid Fine-Needle aspiration biopsy specimens for preoperative risk stratification in papillary thyroid cancer J Clin Oncol 27 18 2009 2977 2982
43. R. Elisei, D. Viola, and L. Torregrossa et al. The BRAF(V600E) mutation is an independent, poor prognostic factor for the outcome of patients with low-risk intrathyroid papillary thyroid carcinoma: single-institution results from a large cohort study J Clin Endocrinol Metab 97 12 2012 4390 4398
44. C. Li, K.C. Lee, and E.B. Schneider et al. BRAF V600E mutation and its association with clinicopathological features of papillary thyroid cancer: a meta-analysis J Clin Endocrinol Metab 97 12 2012 4559 4570
45. M. Eszlinger, J.F. Krane, and E.S. Cibas et al. Molecular analysis of residual ThinPrep material after cytology classification according to the Bethesda System for Reporting Thyroid Cytopathology (TBS) increases sensitivity and allows molecular diagnostics for non-diagnostic samples 83rd Annual meeting of the American thyroid association 111 2013
46. M.N. Nikiforova, A.I. Wald, and S. Roy et al. Targeted next-generation sequencing panel (ThyroSeq) for detection of mutations in thyroid cancer J Clin Endocrinol Metab 98 11 2013 E1852 E1860
47. M.N. Nikiforova, A. Wald, and S.P. Hodak et al. Targeted next-generation sequencing (Thyroseq) for diagnosis of thyroid cancer 83rd Annual meeting of the American thyroid association 73 2013
48. S.M. Wiseman, Z. Haddad, and B. Walker et al. Whole-transcriptome profiling of thyroid nodules identifies expression-based signatures for accurate thyroid cancer diagnosis J Clin Endocrinol Metab 98 10 2013 4072 4079
49. M. Eszlinger, K. Krohn, and A. Kukulska et al. Perspectives and limitations of microarray-based gene expression profiling of thyroid tumors Endocr Rev 28 3 2007 322 338
50. K. Aogi, K. Kitahara, and I. Buley et al. Telomerase activity in lesions of the thyroid: application to diagnosis of clinical samples including fine-needle aspirates Clin Cancer Res 4 8 1998 1965 1970
51. V.J. Bernet, J. Anderson, and Y. Vaishnav et al. Determination of galectin-3 messenger ribonucleic acid overexpression in papillary thyroid cancer by quantitative reverse transcription-polymerase chain reaction J Clin Endocrinol Metab 87 10 2002 4792 4796
52. M.B. Casey, C.M. Lohse, and R.V. Lloyd Distinction between papillary thyroid hyperplasia and papillary thyroid carcinoma by immunohistochemical staining for cytokeratin 19, galectin-3, and HBME-1 Endocr Pathol 14 1 2003 55 60
53. B.R. Haugen, S. Nawaz, and N. Markham et al. Telomerase activity in benign and malignant thyroid tumors Thyroid 7 3 1997 337 342
54. H. Inohara, Y. Honjo, and T. Yoshii et al. Expression of galectin-3 in fine-needle aspirates as a diagnostic marker differentiating benign from malignant thyroid neoplasms Cancer 85 11 1999 2475 2484
55. A. Ippolito, V. Vella, and G.L. La Rosa et al. Immunostaining for Met/HGF receptor may be useful to identify malignancies in thyroid lesions classified suspicious at fine-needle aspiration biopsy Thyroid 11 8 2001 783 787
56. T. Mase, H. Funahashi, and T. Koshikawa et al. HBME-1 immunostaining in thyroid tumors especially in follicular neoplasm Endocr J 50 2 2003 173 177
57. S.J. Raphael The meanings of markers: ancillary techniques in diagnosis of thyroid neoplasia Endocr Pathol 13 4 2002 301 311
58. M.J. Sack, C. Astengo-Osuna, and B.T. Lin et al. HBME-1 immunostaining in thyroid fine-needle aspirations: a useful marker in the diagnosis of carcinoma Mod Pathol 10 7 1997 668 674
59. E. Saggiorato, S. Cappia, and P. De Giuli et al. Galectin-3 as a presurgical immunocytodiagnostic marker of minimally invasive follicular thyroid carcinoma J Clin Endocrinol Metab 86 11 2001 5152 5158
60. J. Lu, G. Getz, and E.A. Miska et al. MicroRNA expression profiles classify human cancers Nature 435 7043 2005 834 838
61. M. Rossing Classification of follicular cell-derived thyroid cancer by global RNA profiling J Mol Endocrinol 50 2 2013 R39 R51
62. P. Pallante, R. Visone, and M. Ferracin et al. MicroRNA deregulation in human thyroid papillary carcinomas Endocr Relat Cancer 13 2 2006 497 508
63. F. Weber, R.E. Teresi, and C.E. Broelsch et al. A limited set of human MicroRNA is deregulated in follicular thyroid carcinoma J Clin Endocrinol Metab 91 9 2006 3584 3591
64. H. He, K. Jazdzewski, and W. Li et al. The role of microRNA genes in papillary thyroid carcinoma Proc Natl Acad Sci U S A 102 52 2005 19075 19080
65. M.N. Nikiforova, G.C. Tseng, and D. Steward et al. MicroRNA expression profiling of thyroid tumors: biological significance and diagnostic utility J Clin Endocrinol Metab 93 5 2008 1600 1608
66. L. Lodewijk, A.M. Prins, and J.W. Kist et al. The value of miRNA in diagnosing thyroid cancer: a systematic review Cancer Biomark 11 6 2012 229 238
67. T. Stokowy, B. Wojtas, and K. Fujarewicz et al. miRNAs with the potential to distinguish follicular thyroid carcinomas from benign follicular thyroid tumors - results of a meta-analysis Horm Metab Res 2013 [Epub ahead of print], PMID: 24446156
68. M. Dettmer, A. Vogetseder, and M.B. Durso et al. MicroRNA expression array identifies novel diagnostic markers for conventional and oncocytic follicular thyroid carcinomas J Clin Endocrinol Metab 98 1 2013 E1 E7
69. L. Thomas Retrospective power analysis Conserv Biol 11 1997 276 280
70. S. Lassalle, V. Hofman, and M. Ilie et al. Can the microRNA signature distinguish between thyroid tumors of uncertain malignant potential and other well-differentiated tumors of the thyroid gland? Endocr Relat Cancer 18 5 2011 579 594
71. H.V. Reddi, P. Madde, and D. Milosevic et al. The putative PAX8/PPARgamma fusion oncoprotein exhibits partial tumor suppressor activity through up-regulation of micro-RNA-122 and dominant-negative PPARgamma activity Genes Cancer 2 1 2011 46 55
72. M. Rossing, R. Borup, and R. Henao et al. Down-regulation of microRNAs controlling tumourigenic factors in follicular thyroid carcinoma J Mol Endocrinol 48 1 2012 11 23
73. D. Chudova, J.I. Wilde, and E.T. Wang et al. Molecular classification of thyroid nodules using high-dimensionality genomic data J Clin Endocrinol Metab 95 12 2010 5296 5304
74. E.K. Alexander, G.C. Kennedy, and Z.W. Baloch et al. Preoperative diagnosis of benign thyroid nodules with indeterminate cytology N Engl J Med 367 8 2012 705 715
75. B. McIver, H.V. Reddi, and L.L. Kosok et al. An independent study of a gene expression classifier (AfirmaTM) in the evaluation of cytologically indeterminate thyroid nodules: initial report 82nd Annual meeting of the American thyroid association 171 2012
76. K.M. Arce, V. Mohan, and P. Desantis et al. Clinical validity and utility of the novel gene expression classifier in thyroid nodules at Cleveland Clinic Florida 83rd Annual meeting of the American thyroid association 110 2013
77. K.N. Patel, and K.S. Heller The benefit of gene expression classifier testing in avoiding surgery on indeterminate thyroid nodules may be less than anticipated 83rd Annual meeting of the American thyroid association 96 2013
78. R.M. Harrell, and D.N. Bimston Surgical utility of afirma: effects of high cancer prevalence and oncocytic cell types in patients with indeterminate thyroid cytology Endocr Pract 2013 1 16
79. E.K. Alexander, M. Schorr, and J. Klopper et al. Multicenter clinical experience with the afirma gene expression classifier J Clin Endocrinol Metab 99 1 2014 119 125
80. H. Li, K.A. Robinson, and B. Anton et al. Cost-effectiveness of a novel molecular test for cytologically indeterminate thyroid nodules J Clin Endocrinol Metab 96 11 2011 E1719 E1726
81. M. Najafzadeh, C.A. Marra, and L.D. Lynd et al. Cost-effectiveness of using a molecular diagnostic test to improve preoperative diagnosis of thyroid cancer Value Health 15 8 2012 1005 1013
82. B. McIver Evaluation of the thyroid nodule Oral Oncol 49 7 2013 645 653
83. C.C. Wang, L. Friedman, and G.C. Kennedy et al. A large multicenter correlation study of thyroid nodule cytopathology and histopathology Thyroid 21 3 2011 243 251
84. P.A. Vanderlaan, J.F. Krane, and E.S. Cibas The frequency of 'atypia of undetermined significance' interpretations for thyroid fine-needle aspirations is negatively correlated with histologically proven malignant outcomes Acta Cytol 55 6 2011 512 517
85. E.S. Cibas, and S.Z. Ali The Bethesda system for reporting thyroid cytopathology Thyroid 19 11 2009 1159 1165
86. R.M. Tuttle, D.W. Ball, and D. Byrd et al. Thyroid carcinoma J Natl Compr Canc Netw 8 11 2010 1228 1274
87. Y.C. Oertel, L. Miyahara-Felipe, and M.G. Mendoza et al. Value of repeated fine needle aspirations of the thyroid: an analysis of over ten thousand FNAs Thyroid 17 11 2007 1061 1066
88. K. Kuma, F. Matsuzuka, and A. Kobayashi et al. Outcome of long standing solitary thyroid nodules World J Surg 16 4 1992 583 587
89. D.J. Lim, J.Y. Kim, and K.H. Baek et al. Natural course of cytologically benign thyroid nodules: observation of ultrasonographic changes Endocrinol Metab Seoul 28 2 2013 110 118
90. L. Yip, C. Farris, and A.S. Kabaker et al. Cost impact of molecular testing for indeterminate thyroid nodule fine-needle aspiration biopsies J Clin Endocrinol Metab 97 6 2012 1905 1912
91. S. Piana, A. Frasoldati, and M. Ferrari et al. Is a five-category reporting scheme for thyroid fine needle aspiration cytology accurate? experience of over 18 000 FNAs reported at the same institution during 1998-2007 Cytopathology 22 3 2010 164 173