Ebru TASTEKİN, Sule CANBERK, Fernando C. SCHMİTT

Follicular Growth Pattern Disease on Thyroid Fine-needle Aspiration Biopsy

Thyroid nodules are a common worldwide health problem and a diagnostic challenge for clinicians and cytopathologists. Follicular growth pattern constitutes the majority of thyroid lesions. Thyroid nodules can be neoplastic or non-neoplastic, and neoplastic nodules can be classified as benign, malignant, or gray zone. Gray zone lesions include different benign and malignant entities that might be resulted in unnecessary thyroidectomies with risk of morbidity and higher health care costs. Depending on the cellularity, most cases might fall into the follicular neoplasia (FN)/ suspicious for FN (SFN) category or follicular lesion of undetermined significance (FLUS) in The Bethesda System for Reporting Thyroid Cytopathology (TBSRTC). Pathologists must be aware of the relationship between this diagnostic category and follow-up patient management and avoid over-diagnosing by mastering the diagnostic criteria.

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Cibas ES, Ali SZ. The 2017 Bethesda System for Reporting Thyroid Cytopathology. Thyroid. 2017;27:1341-1346. [CrossRef]
Trimboli P, Crescenzi A, Giovanella L. Performance of Italian Consensus for the Classification and Reporting of Thyroid Cytology (ICCRTC) in discriminating indeterminate lesions at low and high risk of malignancy. A systematic review and metaanalysis. Endocrine. 2018;60:31-35. [CrossRef]
Rossi ED, Morassi F, Santeusanio G, Zannoni GF, Fadda G. Thyroid fine needle aspiration cytology processed by ThinPrep: an additional slide decreased the number of inadequate results. Cytopathology. 2010;21:97-102. [CrossRef]
Duncan LD, Forrest L, Law WM Jr, Hubbard E, Stewart LE. Evaluation of thyroid fine-needle aspirations: can ThinPrep be used exclusively to appropriately triage patients having a thyroid nodule? Diagn Cytopathol. 2011;39:341-348. [CrossRef]
Ravetto C, Colombo L, Dottorini ME. Usefulness of fine-needle aspiration in the diagnosis of thyroid carcinoma: a retrospective study in 37,895 patients. Cancer. 2000;90:357-363. [CrossRef]
Poller DN, Ibrahim AK, Cummings MH, Mikel JJ, Boote D, Perry M. Fine-needle aspiration of the thyroid. Cancer. 2000;90:239-244. [CrossRef]
Siyed AZ, Cibas ES. The Bethesda System for Reporting Thyroid Cytopathology: Definitions, Criteria and Explanatory Notes, 2nd ed. Cham ham: Springer International Publishing, Switzerland; 2018. [CrossRef]
Guidelines of the Papanicolaou Society of Cytopathology for the examination of fine-needle aspiration specimens from thyroid nodules. The Papanicolaou Society of Cytopathology Task Force on Standards of Practice. Mod Pathol. 1996;9:710-715. [CrossRef]
American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009;19:1167-1214. [CrossRef]
Haugen BR, Alexander EK, Bible KC, et al. 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. 2016;26:1-133. [CrossRef]
Gharib H, Papini E, Valcavi R, et al. American Association of Clinical Endocrinologists and Associazione Medici Endocrinologi medical guidelines for clinical practice for the diagnosis and management of thyroid nodules. Endocr Pract. 2006;12:63-102. Erratum in: Endocr Pract. 2008;14:802-803. [CrossRef]
Cibas ED, Ali SZ; NCI Thyroid FNA State of the Science Conference. The Bethesda system for reporting thyroid cytopathology. Am J Clin Pathol. 2009;132:658-665. [CrossRef]
Baloch ZW, LiVolsi VA, Asa SL, et al. Diagnostic terminology and morphologic criteria for cytologic diagnosis of thyroid lesions: a synopsis of the National Cancer Institute fine-needle aspiration state-of-science conference. Diagn Cytopathol. 2008;36:425-437. [CrossRef
Perros P, Clarke SE, Franklyn J. British Thyroid Association, Royal College of Physicians. Guidelines for the management of thyroid cancer, 2nd ed. Report of the Thyroid Cancer Guidelines Update Group. London: RCP, 2007. [CrossRef]
Lobo C, McQueen A, Beale T, Kocjan G. The UK royal college of pathologists thyroid fine-needle aspiration diagnostic classification is a robust tool for the clinical management of abnormal thyroid nodules. Acta Cytol. 2011;55:499-506. [CrossRef]
Perros P, Boelaert K, Colley S, et al. Guidelines for the management of thyroid cancer. Clin Endocrinol (OXF). 2014;81:1-122. [CrossRef]
Fadda G, Basolo F, Bondi A, et al. Cytological classification of thyroid nodules. Proposal of the SIAPEC-IAP Italian consensus working group. Pathologica. 2010;102:405-408. [CrossRef]
Nardi F, Basolo F, Crescenzi A, et al. Italian consensus for the classification and reporting of thyroid cytology. J Endocrinol Invest. 2014;37:593-599. [CrossRef]
Royal College of Pathologists of Australasia. Thyroid cytology structured reporting protocol. 2 nd ed. 2019. Available at: https://www.rcpa.edu.au/ getattachment/92c429b1-605f-4358-bbeb-26f66084ced9/Protocol-thyroid-FNAcytology.aspx. [CrossRef]
The Bethesda System for reporting thyroid cytopathology. Syed AZ, Cibas ES, editors. New York: Springer; 2010.
Rossi ED, Pusztaszeri M, Schmitt F, Bongiovanni M, Chandra A, Faquin WC. Thyroid FNA: international perspectives from the European congress of cytopathology: can we cross the bridge of classifications? Cancer Cytopathol. 2015;123:207-211. [CrossRef]
Poller DN, Baloch ZW, Fadda G, et al. Thyroid FNA: New classifications and new interpretations. Cancer Cytopathol. 2016;124:457-466. [CrossRef]
Bongiovanni M, Spitale A, Faquin WC, Mazzucchelli L, Baloch ZW. The Bethesda system for reporting thyroid cytopathology: a meta-analysis. Acta Cytol. 2012;56:333- 339. [CrossRef]
Boonyaarunnate T, Olson MT, Ali SZ. ‘Suspicious for a follicular neoplasm’ before and after the Bethesda System for Reporting Thyroid Cytopathology: impact of standardized terminology. Acta Cytol. 2013;57:455-463. [CrossRef]
Olson MT, Boonyaarunnate T, Altinboga AA, Ali SZ. ‘Suspicious for papillary thyroid carcinoma’ before and after The Bethesda System for Reporting Thyroid Cytopathology: impact of standardized terminology. Acta Cytol. 2014;58:15-22. [CrossRef]
Baloch ZW, Mandel SJ, LiVolsi VA. Are we ready to modify the Bethesda thyroid fine-needle aspiration classification scheme? Cancer Cytopathol. 2013;121:171-174. [CrossRef]
Nagarkatti SS, Faquin WC, Lubitz CC, et al. Management of thyroid nodules with atypical cytology on fine-needle aspiration biopsy. Ann Surg Oncol. 2013;20:60-65. [CrossRef]
Olson MT, Clark DP, Erozan YS, Ali SZ. Spectrum of risk of malignancy in subcategories of ‘atypia of undetermined significance’. Acta Cytol. 2011;55:518-525. [CrossRef]
Horne MJ, Chhieng DC, Theoharis C, et al. Thyroid follicular lesion of undetermined significance: Evaluation of the risk of malignancy using the two-tier sub-classification. Diagn Cytopathol. 2012;40:410-415. [CrossRef]
Hyeon J, Ahn S, Shin JH, Oh YL. The prediction of malignant risk in the category “atypia of undetermined significance/follicular lesion of undetermined significance” of the Bethesda System for Reporting Thyroid Cytopathology using subcategorization and BRAF mutation results. Cancer Cytopathol. 2014;122:368-376. [CrossRef]
Dincer N, Balci S, Yazgan A, et al. Follow-up of atypia and follicular lesions of undetermined significance in thyroid fine needle aspiration cytology. Cytopathology. 2013;24:385-390. [CrossRef]
Gocun PU, Karakus E, Bulutay P, Akturk M, Akin M, Poyraz A. What is the malignancy risk for atypia of undetermined significance? Three years’ experience at a university hospital in Turkey. Cancer Cytopathol. 2014;122:604-610. [CrossRef]
Wu HH, Inman A, Cramer HM. Subclassification of “atypia of undetermined significance” in thyroid fine-needle aspirates. Diagn Cytopathol. 2014;42:23-29. [CrossRef]
Rodrigues HG, de Pontes AA, Adan LF. Use of molecular markers in samples obtained from preoperative aspiration of thyroid. Endocr J. 2012;59:417-424. [CrossRef]
Paunovic I, Isic T, Havelka M, Tatic S, Cvejic D, Savin S. Combined immunohistochemistry for thyroid peroxidase, galectin-3, CK19 and HBME-1 in differential diagnosis of thyroid tumors. APMIS. 2012;120:368-379. [CrossRef]
Chiu CG, Strugnell SS, Griffith OL, et al. Diagnostic utility of galectin-3 in thyroid cancer. Am J Pathol. 2010;176:2067-2081. [CrossRef]
Bartolazzi A, Orlandi F, Saggiorato E, et al. Galectin-3-expression analysis in the surgical selection of follicular thyroid nodules with indeterminate fine-needle aspiration cytology: a prospective multicentre study. Lancet Oncol. 2008;9:543-549. [CrossRef]
Prasad ML, Pellegata NS, Huang Y, Nagaraja HN, de la Chapelle A, Kloos RT. Galectin-3, fibronectin-1, CITED-1, HBME-1 and cytokeratin-19 immunohistochemistry is useful for the differential diagnosis of thyroid tumors. Mod Pathol. 2005;18:48-57. [CrossRef]
Rossi ED, Raffaelli M, Minimo C, et al. Immunocytochemical evaluation of thyroid neoplasms on thin-layer smears from fine-needle aspiration biopsies. Cancer. 2005;105:87-95. [CrossRef]
Herrmann ME, LiVolsi VA, Pasha TL, et al. Immunohistochemical expression of galectin-3 in benign and malignant thyroid lesions. Arch Pathol Lab Med. 2002;126:710-713. [CrossRef]
Canberk Ş, Fırat P, Schmitt F. Pitfalls in the Cytological Assessment of Thyroid Nodules. Turk Patoloji Derg. 2015;31 Suppl 1:18-33. [CrossRef]
De May Richard. The Art and science of cytopathology. 2nd ed. Chicago: ASCP;2012. [CrossRef]
Syed AZ, Nayar R, Krane JF, Westra WH. Atlas of Thyroid cytopathology with histopathologic correlations. New York: Demos Medical Publishing; 2014. [CrossRef]
Yang J, Schnadig V, Logrono R, Wasserman PG. Fine-needle aspiration of thyroid nodules: a study of 4703 patients with histologic and clinical correlations. Cancer. 2007;111:306-315. [CrossRef]
Deveci MS, Deveci G, LiVolsi VA, Baloch ZW. Fine-needle aspiration of follicular lesions of the thyroid. Diagnosis and follow-Up. Cytojournal. 2006;3:9. [CrossRef]
Baloch ZW, Fleisher S, LiVolsi VA, Gupta PK. Diagnosis of “follicular neoplasm”: a gray zone in thyroid fine-needle aspiration cytology. Diagn Cytopathol. 2002;26:41- 44. [CrossRef]
Renshaw AA, Wang E, Wilbur D, et al. Interobserver agreement on microfollicules in thyroid fine-needle aspirates. Arch Pathol Lab Med. 2006;130:148-152. [CrossRef]
Faquin WC. Diagnosis and reporting of follicular-patterned thyroid lesions by fine needle aspiration. Head Neck Pathol. 2009;3:82-85. [CrossRef]
Damiani D, Suciu V, Vielh P. Cytopathology of follicular cell nodules. Endocr Pathol. 2015; 26:286-290. [CrossRef]
Baloch ZW, LiVolsi VA. Current role and value of fine-needle aspiration in nodular goitre. Best Pract Res Clin Endocrinol Metab. 2014;28:531-544. [CrossRef]
Clark DP, Faquin WC. Thyroid cytopathology. New York: Springer; 2005. [CrossRef]
Syed AZ, Cibas ES. The Bethesda System for reporting thyroid cytopathology. New York: Springer; 2010. [CrossRef]
Baloch ZW, Fleisher S, LiVolsi VA, Gupta PK. Diagnosis of “follicular neoplasm”: a gray zone in thyroid fine-needle aspiration cytology. Diagn Cytopathol. 2002;26:41- 44. [CrossRef]
Faquin WC, Baloch ZW. Fine-needle aspiration of follicular patterned lesions of the thyroid: Diagnosis, management, and follow-up according to National Cancer Institute (NCI) recommendations. Diagn Cytopathol. 2010;38:731-739. [CrossRef]
Schmitt F. Cytopathology. In: Schmitt, F, ed. Encyclopedia of Pathology. Cham, Switzerland: Springer; 2017:376-379. [CrossRef]
Canberk Ş, Fırat P, Schmitt F. Pitfalls in the cytological assessment of thyroid nodules. Turk Patoloji Derg. 2015;31 Suppl 1:18-33. [CrossRef]
Liu CY, Chen CC, Bychkov A, et al. Constitutive Cytomorphologic Features of Medullary Thyroid Carcinoma Using Different Staining Methods. Diagnostics (Basel). 2021;11:1396. [CrossRef]
Deshpande AH, Bobhate SK. Cytological features of dyshormonogenetic goiter: case report and review of the literature. Diagn Cytopathol. 2005;33:252-254. [CrossRef]
Agarwal AM, Bentz JS, Hungerford R, Abraham D. Parathyroid fine-needle aspiration cytology in the evaluation of parathyroid adenoma: cytologic findings from 53 patients. Diagn Cytopathol. 2009;37:407-410. [CrossRef]
Lastra RR, LiVolsi VA, Baloch ZW. Aggressive variants of follicular cell-derived thyroid carcinomas: a cytopathologist’s perspective. Cancer Cytopathol. 2014;122:484-503. [CrossRef]
Bongiovanni M, Bloom L, Krane JF, et al. Cytomorphologic features of poorly differentiated thyroid carcinoma: a multi-institutional analysis of 40 cases. Cancer. 2009;117:185-194. [CrossRef]
Schmitt FC, Barroca H. Role of ancillary studies in fine-needle aspiration from selected tumors. Cancer Cytopathol. 2012;120:145-160. [CrossRef]
Schmitt FC, Longatto-Filho A, Valent A, Vielh P. Molecular techniques in cytopathology practice. J Clin Pathol. 2008;61:258-267. [CrossRef]
Filho AL, Gonçalves AE, Martinho O, Schmitt FC, Reis RM. Liquid-based cytology in DNA-based molecular research. Anal Quant Cytol Histol. 2009;31:395-400. [CrossRef]
Nikiforova MN, Nikiforov YE. Molecular diagnostics and predictors in thyroid cancer. Thyroid. 2009;19:1351-1361. [CrossRef]
Nikiforov YE, Steward DL, Robinson-Smith TM, et al. Molecular testing for mutations in improving the fine-needle aspiration diagnosis of thyroid nodules. J Clin Endocrinol Metab. 2009;94:2092-2098. [CrossRef]
Ohori NP, Nikiforova MN, Schoedel KE, et al. Contribution of molecular testing to thyroid fine -needle aspiration cytology of “follicular lesion of undetermined significance/atypia of undetermined significance”. Cancer Cytopathol. 2010;118:17- 23. [CrossRef]
Gharib H, Papini E, Valcavi R, et al. American Association of Clinical Endocrinologists and Associazione Medici Endocrinologi medical guidelines for clinical practice for the diagnosis and management of thyroid nodules. Endocr Pract. 2006;12:63-102. [CrossRef]
Baloch ZW, LiVolsi VA, Asa SL, et al. Diagnostic terminology and morphologic criteria for cytologic diagnosis of thyroid lesions: a synopsis of the National Cancer Institute Thyroid Fine-Needle Aspiration State of Science Conference. Diagn Cytopathol. 2008;36:425-437. [CrossRef]
Cibas ES, Ali SZ; NCI Thyroid FNA State of the Science Conference. The Bethesda System For Reporting Thyroid Cytopathology. Am J Clin Pathol. 2001;32:658-665. [CrossRef]
Rossi ED, Morassi F, Santeusanio G, Zannoni GF, Fadda G. Thyroid fine needle aspiration cytology processed by ThinPrep: an additional slide decreased the number of inadequate results. Cytopathology. 2010;21:97-102. [CrossRef]
Cochand-Priollet B, Prat JJ, Polivka M, et al. Thyroid fine needle aspiration: the morphological features on ThinPrep slide preparations. Eighty cases with histological control. Cytopathology. 2003;14:343-349. [CrossRef]
Fadda G, Rossi ED, Raffaelli M,et al. Follicular thyroid neoplasms can be classified as low- and high-risk according to HBME-1 and galectin-3 expression on liquid-based fine-needle cytology. Eur J Endocrinol. 2011;165:447-453. [CrossRef]
de Matos LL, Del Giglio AB, Matsubayashi CO, de Lima Farah M, Del Giglio A, da Silva Pinhal MA. Expression of CK-19, galectin-3 and HBME-1 in the differentiation of thyroid lesions: systematic review and diagnostic meta-analysis. Diagn Pathol. 2012;7:97. [CrossRef]
Paunovic I, Isic T, Havelka M, Tatic S, Cvejic D, Savin S. Combined immunohistochemistry from thyroid peroxidase, galectin-3, CK19 and HBME-1 in differential diagnosis of thyroid tumors. APMIS. 2012;120:368-379. [CrossRef]
Papale F, Cafiero G, Grimaldi A, et al. Galectin-3 expression in thyroid fine needle cytology (t-FNAC) uncertain cases: validation of molecular markers and technology innovation. J Cell Physiol. 2013 228:968-974. [CrossRef]
Bartolazzi A, Orlandi F, Saggiorato E, et al. Italian Thyroid Cancer Study Group (ITCSG). Galectin-3-expression analysis in the surgical selection of follicular thyroid nodules with indeterminate fine-needle aspiration cytology: a prospective multicentre study. Lancet Oncol. 2008;9:543-549. [CrossRef]
Ramkumar S, Sivanandham S. The Combined Utility of HBME-1 and Galectin-3 Immunohistochemistry and BRAF V600E Mutations in the Diagnosis of Papillary Thyroid Carcinoma. Cureus. 2021;13:e20339. [CrossRef]
Abu-Sinna E, Hasan MY, El-Deftar MM, Amer SA, Abdelsalam LO, Nakhla JA. Galectin-3 and HBME-1 Expression on Agarose Cell Blocks from Fine-needle aspirates of Follicular Cell-derived Thyroid Tumors. J Cytol. 2018;35:27-32. [CrossRef]
Fadda G, Rossi ED, Raffaelli M, et al. Follicular thyroid neoplasms can be classified as low- and high-risk according to HBME-1 and Galectin-3 expression on liquidbased fine-needle cytology. Eur J Endocrinol. 2011;165:447-453. [CrossRef]
Margari N, Giovannopoulos I, Pouliakis A, et al. Application of Immunocytochemistry on Cell Block Sections for the Investigation of Thyroid Lesions. Acta Cytol. 2018;62:137-144. [CrossRef]
Chiu CG, Strugnell SS, Griffith OL, et al. Diagnostic utility of galectin-3 in thyroid cancer. Am J Pathol. 2010;176:2067-2081. [CrossRef]
Prasad ML, Pellegata NS, Huang Y, Nagaraja HN, de la Chapelle A, Kloos RT. Galectin-3, fibronectin-1, CITED-1, HBME1 and cytocheratin-19 immunohistochemistry is useful for the differential diagnosis of thyroid tumors. Mod Pathol. 2005;18:48-57. [CrossRef]
Rodrigues HG, de Pontes AA, Adan LF. Use of molecular markers in samples obtained from preoperative aspiration of thyroid. Endocr J. 2012;59:417-424. [CrossRef]
Tastekin E, Keskin E, Can N, et al. CD56, CD57, HBME1, CK19, Galectin-3 and p63 immunohistochemical stains in differentiating diagnosis of thyroid benign/malign lesions and NIFTP. Pol J Pathol. 2019;70:286-294. [CrossRef]
Straccia P, Brunelli C, Rossi ED, et al. The immunocytochemical expression of VE-1 (BRAF V600E-related) antibody identifies the aggressive variants of papillary thyroid carcinoma on liquid-based cytology. Cytopathology. 2019;30:460-467. [CrossRef]
Zhao H, Guo HQ, Zhang ZH, et al. [Value of the detection of BRAF(V600E) gene mutation and protein expression in auxiliary cytological diagnosis of papillary thyroid carcinoma]. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2019;54:18- 22. [CrossRef]
Smith AL, Williams MD, Stewart J, et al. Utility of the BRAF p.V600E immunoperoxidase stain in FNA direct smears and cell block preparations from patients with thyroid carcinoma. Cancer Cytopathol. 2018;126:406-413. [CrossRef]
Zhang Y, Liu L, Liu Y, Cao N, Wang L, Xing C. Clinical significance of immunohistochemistry to detect BRAF V600E mutant protein in thyroid tissues. Medicine (Baltimore). 2021; 100:e25566. [CrossRef]
Parker KG, White MG, Cipriani NA. Comparison of Molecular Methods and BRAF Immunohistochemistry (VE1 Clone) for the Detection of BRAF V600E Mutation in Papillary Thyroid Carcinoma: A Meta-Analysis. Head Neck Pathol. 2020;14:1067- 1079. [CrossRef]
Filho AL, Gonçalves AE, Martinho O, Schmitt FC, Reis RM. Liquid-based cytology in DNA-based molecular research: viability and potential application. Anal Quant Cytol Histol. 2009;31:395-400. [CrossRef]
Rossi ED, Martini M, Capodimonti S, et al. BRAF (V600E) mutation analysis on liquid-based cytology-processed aspiration biopsies predicts bilaterality and lymph node involvement in papillary thyroid microcarcinoma. Cancer Cytopathol. 2013;121:291-297. [CrossRef]
Rossi ED, Martini M, Capodimonti S, et al. Diagnostic and prognostic value of immunocytochemistry and BRAF mutation analysis on liquid-based biopsies of thyroid neoplasms suspicious for carcinoma. Eur J Endocrinol. 2013;168:853-859. [CrossRef]
Nishino M. Molecular cytopathology for thyroid nodules: a reviewof methodology and test performance. Cancer Cytopathol. 2016;124:14-27. [CrossRef]
Nikiforov YE, Steward DL, Robinson-Smith TM, et al. Molecular testing for mutations in improving the fine-needle aspiration diagnosis of thyroid nodules. J Clin Endocrinol Metab. 2009;94:2092-2098. [CrossRef]
Soares P, Trovisco V, Rocha AS, et al. BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene. 2003;22:4578-4580. [CrossRef]
Cheung CC, Carydis B, Ezzat S, Bedard YC, Asa SL. Analysis of ret/PTC gene rearrangements refines the fine-needle aspiration diagnosis of thyroid cancer. J Clin Endocrinol Metab. 2001; 86:2187-2190. [CrossRef]
Ohori NP, Nikiforova MN, Schoedel KE, et al. Contribution of molecular testing to thyroid fine-needle aspiration cytology of “follicular lesion of undetermined significance/atypia of undetermined significance”. Cancer Cytopathol. 2010;118:17- 23. [CrossRef]
Moses W, Weng J, Sansano I,et al. Molecular testing for somatic mutations improves the accuracy of thyroid fine-needle aspiration biopsy. World J Surg. 2010;34:2589- 2594. [CrossRef]
Xing M. BRAF mutation in papillary thyroid cancer: pathogenic role, molecular bases, and clinical implications. Endocrinol Rev. 2007;28:742-762. [CrossRef]
Al-Masri M, Al-Shobaki T, Al-Najjar H, et al. BRAF V600E mutation in papillary thyroid carcinoma: it’s relation to clinical features and oncologic outcomes in a single cancer centre experience. Endocr Connect. 2021;10:1531-1537. [CrossRef]
Lin KL, Wang OC, Zhang XH, Dai XX, Hu XQ, Qu JM. The BRAF mutation is predictive of aggressive clinicopathological characteristics in papillary thyroid microcarcinoma. Ann Surg Oncol. 2010;17:3294-3300. [CrossRef]
Puxeddu E, Durante C, Avenia N, Filetti S, Russo D. Clinical implications of BRAF mutation in thyroid carcinoma. Trends Endocrinol Metab. 2008;19:138-145. [CrossRef]
Musholt TJ, Fottner C, Weber M, et al. Detection of papillary carcinoma by analysis of BRAF and RET/PTC1 mutations in fine-needle aspiration biopsies of thyroid nodules. World J Surg. 2010;34:2595-2603. [CrossRef]
Celik M, Bulbul BY, Ayturk S, et al. The relation between BRAFV600E mutation and clinicopathological characteristics of papillary thyroid cancer. Med Glas (Zenica). 2020;17:30-34. [CrossRef]
Sacks WL, Bose S, Zumsteg ZS, et al. Impact of Afirma gene expression classifier on cytopathology diagnosis and rate of thyroidectomy. Cancer Cytopathol. 2016;124:722-728. [CrossRef]
Nikiforov YE, Carty SE, Chiosea SI, et al. Impact of the multi-gene ThyroSeq next-generation sequencing assay on cancer diagnosis in thyroid nodules with atypia of undetermined significance/follicular lesion of undetermined significance cytology. Cytology Thyroid. 2015; 25:1217-1223. [CrossRef]
Labourier E, Shifrin A, Busseniers AE, et al. 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. 2015;100:2743-2750. [CrossRef]
Nishino M. Molecular cytopathology for thyroid nodules: a review of methodology and test performance. Cancer Cytopathol. 2016;124:14-27. [CrossRef]
McIver B, Castro MR, Morris JC, et al. An independent study of a gene expression classifier (Afirma) in the evaluation of cytologically indeterminate thyroid nodules. J Clin Endocrinol Metab. 2014;99:4069-4077. [CrossRef]
Harrell RM, Bimston DN. Surgical utility of Afirma: effects of high cancer prevalence and oncocytic cell types in patients with indeterminate thyroid cytology. Endocr Pract. 2014; 20:364-369. [CrossRef]
Alvarez-Nuñez F, Bussaglia E, Mauricio D, et al. PTEN promoter methylation in sporadic thyroid carcinomas. Thyroid. 2006;16:17-23. [CrossRef]
Hu S, Liu D, Tufano RP, et al. Association of aberrant methylation of tumor suppressor genes with tumor aggressiveness and BRAF mutation in papillary thyroid cancer. Int J Cancer. 2006; 119:2322-2329. [CrossRef]
Xing M. Gene methylation in thyroid tumorigenesis. Endocrinology. 2007;148:948- 953. [CrossRef]
Schagdarsurengin U, Gimm O, Hoang-Vu C, Dralle H, Pfeifer GP, Dammann R. Frequent epigenetic silencing of the CpG island promoter of RASSF1A in thyroid carcinoma. Cancer Res. 2002;62:3698-3701. [CrossRef]
Nakamura N, Carney JA, Jin L, et al. RASSF1A and NORE1A methylation and BRAFV600E mutations in thyroid tumors. Lab Invest. 2005;85:1065-1075. [CrossRef]
Xing M, Cohen Y, Mambo E, et al. Early occurrence of RASSF1A hypermethylation and its mutual exclusion with BRAF mutation in thyroid tumorigenesis. Cancer Res. 2004;64:1664-1668. [CrossRef]
Canberk S, Lima AR, Pinto M, Máximo V. Translational Potential of Epigenetic-Based Markers on Fine-Needle Aspiration Thyroid Specimens. Front Med (Lausanne). 2021;8:640460. [CrossRef]