DOI: http://dx.doi.org/10.17305/bjbms.2017.2039 | Full Text: [PDF]

Follicular morphological characteristics may be associated with invasion in follicular thyroid neoplasms with papillary-like nuclear features

Nuray Can, Mehmet Celik, Yavuz Atakan Sezer, Filiz Ozyilmaz, Semra Ayturk, Ebru Tastekin, Necdet Sut, Hakan Gurkan, Funda Ustun, Buket Yilmaz Bulbul, Sibel Guldiken, Fulya Oz Puyan

Abstract


The newly proposed nomenclature and diagnostic criteria for encapsulated follicular variant of papillary thyroid carcinoma (EFVPTC), the noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP), could improve the consistency and accuracy of diagnosing this entity. Diagnosis of NIFTP requires evaluation of the complete tumor border or capsule. The presence of tumor invasion in follicular thyroid neoplasms with papillary-like nuclear features has been recently discussed by many authors. In this study, we examined the predictive value and association of follicular morphological characteristics with the tumor invasion. In addition, we analyzed the association between tumor encapsulation and molecular profile in EFVPTC/NIFTP cases. A total of 106 cases of FVPTC were included in the study. The tumors were grouped based on the presence of tumor capsule and characteristics of tumor border, as 1) completely encapsulated tumors without invasion, 2) encapsulated tumors with invasion, 3) infiltrative tumors without a capsule. Clinicopathological features, histomorphological features [nuclear criteria, minor diagnostic features, follicles oriented perpendicular to tumor border/capsule (FOPBC)] and molecular alterations in BRAF, NRAS, and KRAS genes were evaluated. FOPBC were significantly more frequently seen in encapsulated tumors with invasion (p = 0.008). The nuclear features were not associated with the presence of encapsulation and characteristics of tumor border. BRAF mutation was more frequent in infiltrative tumors, while NRAS mutation was more frequent in encapsulated tumors, but the results were not statistically significant (p = 0.917). In conclusion, FOPBC histomorphological feature may be associated with tumor invasion in EFVPTC/NIFTP. Additionally, BRAF/KRAS/NRAS mutation analysis may prevent inadequate treatment in these patients.


Keywords


Noninvasive follicular thyroid neoplasm with papillary-like nuclear features; NIFTP; EFVPTC; histomorphological features; follicular variant of papillary thyroid carcinoma; FVPTC; NRAS; BRAF; mutation

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References


Shi X, Liu R, Basolo F, Giannini R, Shen X, Teng D, et al. Differential clinicopathological risk and prognosis of major papillary thyroid cancer variants. J Clin Endocrinol Metab 2016; 101(1):264-74. https://doi.org/10.1210/jc.2015-2917.

Rossi ED, Bizzarro T, Martini M, Capodimonti S, Sarti D, Cenci T, et al. The evaluation of miRNAs on thyroid FNAC: The promising role of miR-375 in follicular neoplasms. Endocrine 2016;54(3):723-32. https://doi.org/10.1007/s12020-016-0866-0.

Nikiforov YE, Seethala RR, Tallini G, Baloch ZW, Basolo F, Thompson LD, et al. Nomenclature revision for encapsulated follicular variant of papillary thyroid carcinoma: A paradigm shift to reduce overtreatment of indolent tumors. JAMA Oncol 2016;2(8):1023-9. https://doi.org/10.1001/jamaoncol.2016.0386.

Sak SD. Variants of papillary thyroid carcinoma: Multiple faces of a familiar tumor. Turk Patoloji Derg 2015;31(Suppl 1):34-47. https://doi.org/10.5146/tjpath.2015.01313.

Taconet S, Bosq J, Hartl D, Schlumberger M, Leboulleux S, Scoazec JY, et al. Composite mucoepidermoid carcinoma and columnar cell variant of papillary carcinoma of the thyroid: A case report and review of the literature. Int J Surg Pathol 2016;24(4):336-40. https://doi.org/10.1177/1066896915626281.

Kakudo K, Bai Y, Liu Z, Li Y, Ito Y, Ozaki T. Classification of thyroid follicular cell tumors: With special reference to borderline lesions. Endocr J 2012;59(1):1-12. https://doi.org/10.1507/endocrj.EJ11-0184.

Ganly I, Wang L, Tuttle RM, Katabi N, Ceballos GA, Harach HR, et al. Invasion rather than nuclear features correlates with outcome in encapsulated follicular tumors: Further evidence for the reclassification of the encapsulated papillary thyroid carcinoma follicular variant. Hum Pathol 2015;46(5):657-64. https://doi.org/10.1016/j.humpath.2015.01.010.

Lindsay S. Carcinoma of the thyroid gland. A clinical and pathologic study of 293 patients at the University of California Hospital. Springfield, IL: Charles C. Thomas; 1960.

Chem KT, Rosai J. Follicular variant of thyroid papillary carcinoma: A clinicopathologic study of six cases. Am J Surg Pathol 1977;1(2):123-30.

https://doi.org/10.1097/00000478-197706000-00003.

Liu L, Singh B, Tallini G, Carlson DL, Katabi N, Shaha A, et al. Follicular variant of papillary thyroid carcinoma: A clinicopathologic study of a problematic entity. Cancer 2006;107(6):1255-64. https://doi.org/10.1002/cncr.22138.

Elsheikh TM, Asa SL, Chan JK, DeLellis RA, Heffess CS, LiVolsi VA, et al. Interobserver and intraobserver variation among experts in the diagnosis of thyroid follicular lesions with borderline nuclear features of papillary carcinoma. Am J Clin Pathol 2008;130(5):736-44. https://doi.org/10.1309/AJCPKP2QUVN4RCCP.

Ertek S, Yılmaz NC, Cicero AF, Vurupalmaz Ö, Demiröz AS, Erdoğan G. Increasing diagnosis of thyroid papillary carcinoma follicular variant in south-east Anatolian region: Comparison of characteristics of classical papillary and follicular variant thyroid cancers. Endocr Pathol 2012;23(3):157-60. https://doi.org/10.1007/s12022-012-9216-9.

Yu XM, Schneider DF, Leverson G, Chen H, Sippel RS. Follicular variant of papillary thyroid carcinoma is a unique clinical entity: A population-based study of 10,740 cases. Thyroid 2013;23(10):1263-8. https://doi.org/10.1089/thy.2012.0453.

Ito Y, Hirokawa M, Uruno T, Kihara M, Higashiyama T, Takamura Y, et al. Prevalence and biological behaviour of variants of papillary thyroid carcinoma: Experience at a single institute. Pathology 2008;40(6):617-22. https://doi.org/10.1080/00313020802320630.

Agrawal N, Akbani R, Aksoy BA, Ally A, Arachchi H, Asa SL, et al. Integrated genomic characterization of papillary thyroid carcinoma. Cell 2014;159(3):676-90. https://doi.org/10.1016/j.cell.2014.09.050.

Jung CK, Little MP, Lubin JH, Brenner AV, Wells SA Jr, Sigurdson AJ, et al. The increase in thyroid cancer incidence during the last four decades is accompanied by a high frequency of BRAF mutations and a sharp increase in RAS mutations. J Clin Endocrinol Metab 2014;99(2):E276-85. https://doi.org/10.1210/jc.2013-2503.

Thompson LD. Ninety-four cases of encapsulated follicular variant of papillary thyroid carcinoma: A name change to Noninvasive Follicular Thyroid Neoplasm with Papillary-like Nuclear Features would help prevent overtreatment. Mod Pathol 2016;29(7):698-707. https://doi.org/10.1038/modpathol.2016.65.

Kakudo K, Bai Y, Liu Z, Ozaki T. Encapsulated papillary thyroid carcinoma, follicular variant: A misnomer. Pathol Int 2012;62(3):155-60.

https://doi.org/10.1111/j.1440-1827.2011.02773.x.

Rivera M, Tuttle RM, Patel S, Shaha A, Shah JP, Ghossein RA. Encapsulated papillary thyroid carcinoma: A clinico-pathologic study of 106 cases with emphasis on its morphologic subtypes (histologic growth pattern). Thyroid 2009;19(2):119-27. https://doi.org/10.1089/thy.2008.0303.

Yip L, Nikiforova MN, Yoo JY, McCoy KL, Stang MT, Armstrong MJ, et al. Tumor genotype determines phenotype and disease-related outcomes in thyroid cancer: A study of 1510 patients. Ann Surg 2015;262(3):519-55. https://doi.org/10.1097/SLA.0000000000001420.

Zhu Z, Gandhi M, Nikiforova MN, Fischer AH, Nikiforov YE. 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 2003;120(1):71-7. https://doi.org/10.1309/ND8D9LAJTRCTG6QD.

Xing M, Westra WH, Tufano RP, Cohen Y, Rosenbaum E, Rhoden KJ, et al. BRAF mutation predicts a poorer clinical prognosis for papillary thyroid cancer. J Clin Endocrinol Metab 2005;90(12):6373-9. https://doi.org/10.1210/jc.2005-0987.

Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, 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):1-133. https://doi.org/10.1089/thy.2015.0020.

Bullock M. Protocol for the examination of specimens from patients with carcinomas in the thyroid gland 2016 based on AJCC/UICC TNM. 7th ed. College of American Pathologists (CAP); 2016.

Mete O, Asa SL. Pathological definition and clinical significance of vascular invasion in thyroid carcinomas of follicular epithelial derivation. Mod Pathol 2011;24(12):1545-52. https://doi.org/10.1038/modpathol.2011.119.

Sezer A, Celik M, Yilmaz Bulbul B, Can N, Tastekin E, Ayturk S, et al. Relationship between lymphovascular invasion and clinicopathological features of papillary thyroid carcinoma. Bosn J Basic Med Sci 2017;17(2):144-51. https://doi.org/10.17305/bjbms.2017.1924.

Blanchard C, Brient C, Volteau C, Sebag F, Roy M, Drui D, et al. Factors predictive of lymph node metastasis in the follicular variant of papillary thyroid carcinoma. Br J Surg 2013;100(10):1312-7. https://doi.org/10.1002/bjs.9210.

Walts AE, Mirocha JM, Bose S. Follicular variant of papillary thyroid carcinoma (FVPTC): Histological features, BRAF V600E mutation, and lymph node status. J Cancer Res Clin Oncol 2015;141(10):1749-56. https://doi.org/10.1007/s00432-015-1939-9.

Xu B, Ghossein R. Encapsulated thyroid carcinoma of follicular cell origin. Endocr Pathol 2015;26(3):191-9. https://doi.org/10.1007/s12022-015-9376-5.

McFadden DG, Dias-Santagata D, Sadow PM, Lynch KD, Lubitz C, Donovan SE, et al. Identification of oncogenic mutations and gene fusions in the follicular variant of papillary thyroid carcinoma. J Clin Endocrinol Metab 2014;99(11):E2457-62. https://doi.org/10.1210/jc.2014-2611.

Rivera M, Ricarte-Filho J, Knauf J, Shaha A, Tuttle M, Fagin JA, et al. Molecular genotyping of papillary thyroid carcinoma follicular variant according to its histological subtypes (encapsulated vs infiltrative) reveals distinct BRAF and RAS mutation patterns. Mod Pathol 2010;23(9):1191-1200. https://doi.org/10.1038/modpathol.2010.112.

Howitt BE, Jia Y, Sholl LM, Barletta JA. Molecular alterations in partially-encapsulated or well-circumscribed follicular variant of papillary thyroid carcinoma. Thyroid 2013;23(10): 1256-62. https://doi.org/10.1089/thy.2013.0018.

Cho U, Mete O, Kim MH, Bae JS, Jung CK. Molecular correlates and rate of lymph node metastasis of non-invasive follicular thyroid neoplasm with papillary-like nuclear features and invasive follicular variant papillary thyroid carcinoma: The impact of rigid criteria to distinguish non-invasive follicular thyroid neoplasm with papillary-like nuclear features. Mod Pathol 2017;30(6):810-25. https://doi.org/10.1038/modpathol.2017.9.


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