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Endocrine Pathology

, Volume 29, Issue 4, pp 351–356 | Cite as

Cytomorphological Analysis of Thyroid Nodules Diagnosed as Follicular Variant of Papillary Thyroid Carcinoma: a Fine Needle Aspiration Study of Diagnostic Clues in 42 Cases and the Impact of Using Bethesda System in Reporting—an Institutional Experience

  • Levent Trabzonlu
  • Nadir Paksoy
Article

Abstract

Follicular variant of papillary thyroid carcinoma (FVPTC) is the second most common subtype of papillary thyroid carcinoma (PTC) after classical PTC (cPTC). Follicular thyroid lesions such as follicular adenomas/carcinomas, FVPTC, and noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) pose some diagnostic challenges for FNAC. In this study, we aimed to explore whether FNAC can demonstrate diagnostic clues by re-evaluating cytology slides from histopathologically diagnosed FVPTC cases. A total of 42 patients were enrolled in this study: patients were diagnosed with FVPTC via surgical resection between 2006 and 2016, and all patients were subjected to preoperative FNAC, which was conducted at either a private center or at the teaching hospital of Kocaeli University and reported by the same cytopathologist (NP). Clinical and cytomorphological characteristics were reviewed by both authors .Most cases (76.2%) are diagnosed either Bethesda IV or V. The majority of cases had a high cellularity (38/42; 90.5%), and the most frequent observations were monolayer and large syncytial groups of cells (95.2%). While microfollicular structures were observed in 30 (71.4%) cases, nuclear crowding and large naked nuclei were observed in all cases. Nuclear grooves were sparsely detected in 23 (54.8%) cases, and nuclear pseudoinclusions were detected in only six (14.3%) cases. Because thyrocytes often have a mixed architecture in FVPTC, despite a distinct follicular morphology, we believe that nuclear overcrowding, enlargement, and hyperchromasia in cases presenting with increased cellularity are notable clues for the cytodiagnosis of FVPTC. We believe that the primary aim of FNAC in such cases is to give preoperative diagnosis as either category IV or V. Nuclear crowding, monolayered clusters with large syncytial formations, nuclear enlargement, and hyperchromasia are notable cytomorphologic clues for the diagnosis of FVPTC on FNAC.

Keywords

Fine needle aspiration cytology Thyroid neoplasm Follicular variant of papillary thyroid carcinoma (FVPTC) Noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) Cytodiagnostic clues 

Notes

Authorship

Levent Trabzonlu: methodology, software, formal analysis, investigation, resources, data curation, writing—original draft. Nadir Paksoy: conceptualization, formal analysis, resources, writing—review and editing, supervision, and project administration.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

Informed Consent

We state that our study is based on archival cyto-histopathologic slides and reports in which no human investigation has been involved. No informed consent is required.

References

  1. 1.
    Clary KM, Condel JL, Liu Y, Johnson DR, Grzybicki DM, Raab SS (2005) Interobserver variability in the fine needle aspiration biopsy diagnosis of follicular lesions of the thyroid gland. Acta Cytol 49:378–382CrossRefGoogle Scholar
  2. 2.
    Nikiforov YE, Seethala RR, Tallini G, Baloch ZW, Basolo F, Thompson LDR, Barletta JA, Wenig BM, al Ghuzlan A, Kakudo K, Giordano TJ, Alves VA, Khanafshar E, Asa SL, el-Naggar AK, Gooding WE, Hodak SP, Lloyd RV, Maytal G, Mete O, Nikiforova MN, Nosé V, Papotti M, Poller DN, Sadow PM, Tischler AS, Tuttle RM, Wall KB, LiVolsi VA, Randolph GW, Ghossein RA (2016) Nomenclature revision for encapsulated follicular variant of papillary thyroid carcinoma: a paradigm shift to reduce overtreatment of indolent tumors. JAMA Oncol 2:1023–1029CrossRefGoogle Scholar
  3. 3.
    Daniels G (2011) What if many follicular variant papillary thyroid carcinomas are not malignant? A review of follicular variant papillary thyroid carcinoma and aproposal for a new classification. Endocr Pract 17:768–787CrossRefGoogle Scholar
  4. 4.
    Lloyd R V, Erickson LA, Casey MB, Lam KY, Lohse CM, Asa SL, Chan JKC, DeLellis RA, Harach HR, Kakudo K, LiVolsi VA, Rosai J, Sebo TJ, Sobrinho-Simoes M, Wenig BM, Lae ME (2004) Observer variation in thediagnosis of follicular variant of papillary thyroid carcinoma. Am J Surg Path:1336–1340, 28CrossRefGoogle Scholar
  5. 5.
    Baloch ZW, LiVolsi VA (2002) Follicular-patterned lesions of the thyroid. Am J Clin Pathol 117:143–150CrossRefGoogle Scholar
  6. 6.
    Howitt BE, Jia Y, Sholl LM, Barletta JA (2013) Molecular alterations in partially encapsulated or well-circumscribed follicular variant of papillary thyroid carcinoma.Thyroid 23:1256–1262CrossRefGoogle Scholar
  7. 7.
    Rivera M, Ricarte-Filho J, Knauf J, Shaha A, Tuttle M, Fagin JA, Ghossein RA (2010) 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 23:1191–1200CrossRefGoogle Scholar
  8. 8.
    Aron M, Mallik A, Verma K. Fine needle aspiration cytology of follicular variant of papillary carcinoma of the thyroid: Morphologic pointers to its diagnosis. (2006) Acta Cytol 50: 663–668CrossRefGoogle Scholar
  9. 9.
    Zacks JF, de las Morenas A, Beazley RM, O’Brien MJ (1998) Fine-needle aspiration cytology diagnosis of colloid nodule versus follicular variant of papillary carcinoma of the thyroid. Diagn Cytopathol 18:87–90CrossRefGoogle Scholar
  10. 10.
    Ylagan LR, Dehner LP, Huettner PC, Lu D (2004) Columnar cell variant of papillary thyroid carcinoma. Report of a case with cytologic findings. Acta Cytol 48:73–77CrossRefGoogle Scholar
  11. 11.
    Nair M, Kapila K, Karak AK, Verma K (2011) Papillary carcinoma of the thyroid and its variants: a cytohistological correlation. Diagn Cytopathol 24:167–173CrossRefGoogle Scholar
  12. 12.
    Manivannan P, Siddaraju N, Gopalakrsishnan S (2014) A systematic approach to assess the strengths and limitations of cytomorphology in the diagnosis of the follicular variant of papillary thyroid carcinoma. Cytopathology 25:190–198CrossRefGoogle Scholar
  13. 13.
    Strickland KC, Vivero M, Jo VY, Lowe AC, Hollowell M, Qian X, Wieczorek TJ, French CA, Teot LA, Sadow PM, Alexander EK, Cibas ES, Barletta JA, Krane JF (2016) Pre-operative cytologic diagnosis of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP): A prospective analysis. Thyroid 26:1466–1471CrossRefGoogle Scholar
  14. 14.
    Mesonero CE, Jugle JE, Wilbur DC, Nayar R (1998) Fine-needle aspiration of the macrofollicular and microfollicular subtypes of the follicular variant of papillary carcinoma of the thyroid. Cancer 84:235–244CrossRefGoogle Scholar
  15. 15.
    Baloch ZW, Gupta PK, Yu GH, Sack MJ, LiVolsi VA (1999) Follicular variant of papillary carcinoma. Cytologic and histologic correlation. Am J Clin Pathol 111:216–222CrossRefGoogle Scholar
  16. 16.
    Miller JM, Hamburger JI, Kini SR (1981) The needle biopsy diagnosis of papillary thyroid carcinoma. Cancer 48:989–993CrossRefGoogle Scholar
  17. 17.
    Ustun B, Chhieng D, Prasad ML, Holt E, Hammers L, Carling T, Udelsman R, Adeniran AJ (2014) Follicular variant of papillary thyroid carcinoma: accuracy of FNA diagnosis and implications for patient management. Endocr Pathol 25:257–264CrossRefGoogle Scholar
  18. 18.
    Kesmodel S, Terhune KP, Canter RJ, Mandel SJ, LiVolsi V, Baloch ZW, Fraker DL (2003) The diagnostic dilemma of follicular variant of papillary thyroid carcinoma. Surgery 134:1005–1012CrossRefGoogle Scholar
  19. 19.
    Lin H-S, Komisar A, Opher E, Blaugrund SM (2000) Follicular variant of papillary carcinoma: The diagnostic limitations of preoperative fine-needle aspiration and intraoperative frozen section evaluation. Laryngoscope 110:1431–1436CrossRefGoogle Scholar
  20. 20.
    Logani S, Gupta PK, LiVolsi VA, Mandel S, Baloch ZW (2000) Thyroid nodules with FNA cytology suspicious for follicular variant of papillary thyroid carcinoma: follow-up and management. Diagn Cytopathol 23:380–385CrossRefGoogle Scholar
  21. 21.
    Jain M, Khan A, Patwardhan N, Reale F, Safran M (2001) Follicular variant of papillary thyroid carcinoma: a comparative study of histopathologic features and cytology results in 141 patients. Endocr Pract 7:79–84CrossRefGoogle Scholar
  22. 22.
    Ibrahim AA, Wu HH (2016) Fine-needle aspiration cytology of noninvasive follicular variant of papillary thyroid carcinoma is cytomorphologically distinct from the invasive counterpart. Am J Clin Pathol 146:373–377CrossRefGoogle Scholar
  23. 23.
    Maletta F, Massa F, Torregrossa L, Duregon E, Casadei GP, Basolo F, Tallini G, Volante M, Nikiforov YE, Papotti M (2016) Cytological features of “noninvasive follicular thyroid neoplasm with papillary-like nuclear features” and their correlation with tumor histology. Hum Pathol 54:134–142CrossRefGoogle Scholar
  24. 24.
    Brandler TC, Zhou F, Liu CZ, Cho M, Lau RP, Simsir A, Patel KN, Sun W (2017) Can noninvasive follicular thyroid neoplasm with papillary-like nuclear features be distinguished from classic papillary thyroid carcinoma and follicular adenomas by fine-needle aspiration? Cancer Cytopathol 125:378–388CrossRefGoogle Scholar
  25. 25.
    Mito JK, Alexander EK, Angell TE el al (2017) A modified reporting approach for thyroid FNA in the NIFTP era: A 1-year institutional experience. Cancer Cytopathol 125: 854–864CrossRefGoogle Scholar
  26. 26.
    Song SJ, LiVolsi VA, Montone K, Baloch Z (2017) Pre-operative features of non-invasive follicular thyroid neoplasms with papillary-like nuclear features: an analysis of their cytological,Gene-Expression Classifier and sonographic findings. Cytopathology 28: 488–494CrossRefGoogle Scholar
  27. 27.
    Cibas ES, Ali SZ (2017) The 2017 Bethesda system for reporting thyroid cytopathology.Thyroid 27:1341–1346CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Pathology, Faculty of MedicineKocaeli UniversityIzmitTurkey
  2. 2.Pathology DepartmentThe Johns Hopkins HospitalBaltimoreUSA
  3. 3.Dr Paksoy’s Private Cytopathology/FNA PracticeIzmitTurkey

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