J Pathol Transl Med.  2018 Mar;52(2):110-120. 10.4132/jptm.2018.01.17.

Cytological Features That Differentiate Follicular Neoplasm from Mimicking Lesions

Affiliations
  • 1Department of Pathology, Korea Cancer Center Hospital, Korea Institute of Radiological and Medical Sciences (KIRAMS), Seoul, Korea.
  • 2Laboratory of Radiation Pathology, Korea Institute of Radiological and Medical Sciences (KIRAMS), Seoul, Korea. sslee@kirams.re.kr

Abstract

BACKGROUND
It is difficult to correctly diagnose follicular neoplasms (FNs) on fine-needle aspiration cytology (FNAC) because it shares many cytological features with other mimicking lesions. The aim of this study was to identify the cytological features that differentiate FNs from mimicking lesions.
METHODS
We included the cytological slides from 116 cases of thyroid FN diagnosed on FNAC, and included their subsequent histological diagnoses. We evaluated the cytological architectural pattern and nuclear features of the lesions according to their histological groups.
RESULTS
The final histological diagnoses of the 116 cases varied, and included 51 FNs (44%), 47 papillary thyroid carcinomas (40%) including follicular variant, and seventeen cellular nodular hyperplasias (15%). Regardless of the final histological diagnosis, microfollicular pattern was observed in most cases. On the other hand, trabecular pattern was identified in 34% of FNs, but not in any other lesions. Additionally, elongated nuclei and ground glass chromatin were found in only some papillary thyroid carcinomas.
CONCLUSIONS
This study shows that the trabecular pattern is a representative cytological feature of FNs that can be used to distinguish FNs from mimicking lesions. In addition, nuclear shape and chromatin pattern can be used to further confirm the diagnosis of FNs from mimicking lesions through FNAC.

Keyword

Follicular neoplasm; Fine needle aspiration cytology; Differential diagnosis

MeSH Terms

Biopsy, Fine-Needle
Chromatin
Diagnosis
Diagnosis, Differential
Glass
Hand
Hyperplasia
Thyroid Gland
Thyroid Neoplasms
Chromatin

Figure

  • Fig. 1. Histological and cytological features of thyroid neoplasm. (A, B) Histological features of follicular adenoma. (A) The tumor is enclosed in a thick fibrous capsule. (B) The architectural pattern is follicular, and cells are uniform, round and dark. (C) Cytological features of follicular adenoma. Abundant follicular cells are seen, with little colloid. (D, E) Histological features of follicular carcinoma. (D) Vascular invasion in fibrous capsule of follicular carcinoma. (E) Colloid-containing well-formed follicles. (F) Cytological feature of follicular carcinoma. Note that microfollicles show three dimensional branching cellular clusters with trabecular pattern. (G, H) Histological features of follicular variant of papillary carcinoma. (G) The tumor resembles follicular neoplasm. (H) Nuclei are round to ovoid, similar to follicular neoplasm but show slight enlargement and overlapping. (I) Cytoloigcal feature of papillary carcinoma. Monolayer branching sheet of papillary carcinoma is compared with three-dimensional branching cluster of follicular carcinoma. (J, K) Histological features of nodular hyperplasia. Follicles are of varying sizes with abundant colloid. (L) Aspirate of nodular hyperplasia shows flat sheets of uniform follicular cells and colloid.

  • Fig. 2. Microfollicular pattern (A–C) and multilayer rosettes (D–F) are found not only in follicular neoplasm but also in nodular hyperplasia or follicular variant of papillary carcinoma. (A, D) Follicular neoplasm. (B, E) Follicular variant of papillary carcinoma. (C, F) Nodular hyperplasia.

  • Fig. 3. Different features of cell clusters in follicular neoplasm (FN), follicular variant of papillary thyroid carcinoma (FVPTC), and nodular hyperplasia. (A, B) Trabecular pattern in FN. (C) Branching cell sheets in FN. Branching fragments of FN show ribbon-forming overlapped follicular cells. Note the three-dimensional arrangement of follicular cells of FN (C), which is contrasted with monolayer branching sheet of FVPTC (D). (E) Multilayered cellular ball clusters of FN show branching and trabecular pattern. (F) On the other hand, cell ball clusters in NH show no branching pattern with large non-branching cellular sheet in the colloid background.

  • Fig. 4. Nuclear features of follicular neoplasm (FN) and nodular hyperplasia (NH). The nuclear features of FN (A) and NH (B) are similar. Both have round nuclei with microgranular chromatin and nuclear grooves (arrows). However, note the difference that FN (A) shows a three-dimensional arrangement and slightly hyperchromatic nuclei but NH (B). NH has monolayer honeycomb sheets of follicular cells that do not overlap.

  • Fig. 5. Nuclear features of follicular neoplasm (FN) and follicular variant of papillary thyroid carcinoma (FVPTC). Please note the subtle difference of nuclear shape and chromatin between follicular carcinoma (A, C) and FVPTC (B, D). (A, C) In FN, nuclei are round to ovoid and chromatin is finely granular rather than ground glass or vesicular pattern. (B, D) Nuclei in FVPTC are slightly elongated (arrow) and have a ground-glass appearing chromatin pattern.


Reference

1. Hamberger B, Gharib H, Melton LJ 3rd, Goellner JR, Zinsmeister AR. Fine-needle aspiration biopsy of thyroid nodules. Impact on thyroid practice and cost of care. Am J Med. 1982; 73:381–4.
2. Yassa L, Cibas ES, Benson CB, et al. Long-term assessment of a multidisciplinary approach to thyroid nodule diagnostic evaluation. Cancer. 2007; 111:508–16.
Article
3. Cibas ES, Ali SZ. The Bethesda System for Reporting Thyroid Cytopathology. Thyroid. 2009; 19:1159–65.
Article
4. Nikiforov YE, Seethala RR, Tallini G, et al. Nomenclature revision for encapsulated follicular variant of papillary thyroid carcinoma: a paradigm shift to reduce overtreatment of indolent tumors. JAMA Oncol. 2016; 2:1023–9.
5. Liu J, Singh B, Tallini G, et al. Follicular variant of papillary thyroid carcinoma: a clinicopathologic study of a problematic entity. Cancer. 2006; 107:1255–64.
6. Greaves TS, Olvera M, Florentine BD, et al. Follicular lesions of thyroid: a 5-year fine-needle aspiration experience. Cancer. 2000; 90:335–41.
7. 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.
8. Wu HH, Rose C, Elsheikh TM. The Bethesda system for reporting thyroid cytopathology: An experience of 1,382 cases in a community practice setting with the implication for risk of neoplasm and risk of malignancy. Diagn Cytopathol. 2012; 40:399–403.
9. Faquin WC. Diagnosis and reporting of follicular-patterned thyroid lesions by fine needle aspiration. Head Neck Pathol. 2009; 3:82–5.
Article
10. 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; 111:306–15.
Article
11. Brandler TC, Zhou F, Liu CZ, et al. 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. 2017; 125:378–88.
Article
12. Bizzarro T, Martini M, Capodimonti S, et al. Young investigator challenge: the morphologic analysis of noninvasive follicular thyroid neoplasm with papillary-like nuclear features on liquid-based cytology: Some insights into their identification. Cancer Cytopathol. 2016; 124:699–710.
Article
13. Rossi ED, Bizzarro T, Martini M, Larocca LM, Schmitt F, Vielh P. Cytopathology of follicular cell nodules. Adv Anat Pathol. 2017; 24:45–55.
Article
14. Clark DP, Faquin WC. Thyroid cytopathology. New York: Springer;2005. p. 131.
15. Krane JF, Alexander EK, Cibas ES, Barletta JA. Coming to terms with NIFTP: a provisional approach for cytologists. Cancer Cytopathol. 2016; 124:767–72.
Article
16. Maletta F, Massa F, Torregrossa L, et al. Cytological features of “noninvasive follicular thyroid neoplasm with papillary-like nuclear features” and their correlation with tumor histology. Hum Pathol. 2016; 54:134–42.
Article
17. Yoo C, Choi HJ, Im S, et al. Fine needle aspiration cytology of thyroid follicular neoplasm: cytohistologic correlation and accuracy. Korean J Pathol. 2013; 47:61–6.
Article
18. Deka L, Gupta S, Gupta R, Gupta K, Kaur CJ, Singh SS. Nuclear morphometry and texture analysis on cytological smears of thyroid neoplasms: a study of 50 cases. Malays J Pathol. 2017; 39:33–7.
19. Ho AS, Sarti EE, Jain KS, et al. Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS). Thyroid. 2014; 24:832–9.
Article
20. Song JY, Chu YC, Kim L, Park IS, Han JY, Kim JM. Reclassifying formerly indeterminate thyroid FNAs using the Bethesda system reduces the number of inconclusive cases. Acta Cytol. 2012; 56:122–9.
Article
21. Shi Y, Ding X, Klein M, et al. Thyroid fine-needle aspiration with atypia of undetermined significance: a necessary or optional category? Cancer. 2009; 117:298–304.
22. 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; 40:410–5.
Article
23. 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; 24:385–90.
Article
Full Text Links
  • JPTM
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr