Journal of Pathology and Translational Medicine

Original Articles

Cytological Features That Differentiate Follicular Neoplasm from Mimicking Lesions: Kanghee Han, Hwa-Jeong Ha, Joon Seog Kong, Jung-Soon Kim, Jae Kyung Myung, Jae Soo Koh, Sunhoo Park, Myung-Soon Shin, Woo-Tack Song, Hye Sil Seol, Seung-Sook Lee; J Pathol Transl Med. 2018;52(2):110-120. Published online January 29, 2018; DOI: https://doi.org/10.4132/jptm.2018.01.17

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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.

Citations

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Diagnostic implication of thyroid spherules for cytological diagnosis of thyroid nodules
Heeseung Sohn, Kennichi Kakudo, Chan Kwon Jung
Cytopathology.2024; 35(3): 383. CrossRef
Using Deep Convolutional Neural Networks for Enhanced Ultrasonographic Image Diagnosis of Differentiated Thyroid Cancer
Wai-Kin Chan, Jui-Hung Sun, Miaw-Jene Liou, Yan-Rong Li, Wei-Yu Chou, Feng-Hsuan Liu, Szu-Tah Chen, Syu-Jyun Peng
Biomedicines.2021; 9(12): 1771. CrossRef
The Role of Fine Needle Aspiration Biopsy with Bethesda System in the Evaluation of Thyroid Nodules
Gizem AKKAŞ AKGÜN, Figen ASLAN
Anadolu Kliniği Tıp Bilimleri Dergisi.2021; 26(1): 23. CrossRef
Comprehensive DNA Methylation Profiling Identifies Novel Diagnostic Biomarkers for Thyroid Cancer
Jong-Lyul Park, Sora Jeon, Eun-Hye Seo, Dong Hyuck Bae, Young Mun Jeong, Yourha Kim, Ja Seong Bae, Seon-Kyu Kim, Chan Kwon Jung, Yong Sung Kim
Thyroid.2020; 30(2): 192. CrossRef
Preoperative diagnostic categories of fine needle aspiration cytology for histologically proven thyroid follicular adenoma and carcinoma, and Hurthle cell adenoma and carcinoma: Analysis of cause of under- or misdiagnoses
Hee Young Na, Jae Hoon Moon, June Young Choi, Hyeong Won Yu, Woo-Jin Jeong, Yeo Koon Kim, Ji-Young Choe, So Yeon Park, Paula Soares
PLOS ONE.2020; 15(11): e0241597. CrossRef

The Diagnostic Usefulness of HMGA2, Survivin, CEACAM6, and SFN/14-3-3 δ in Follicular Thyroid Carcinoma: Min Hye Jang, Kyeong Cheon Jung, Hye Sook Min; J Pathol Transl Med. 2015;49(2):112-117. Published online March 12, 2015; DOI: https://doi.org/10.4132/jptm.2015.01.31

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Abstract PDF

Background
Follicular thyroid carcinoma (FTC) is the second most common thyroid malignancy and its differential diagnosis includes follicular adenoma (FA) and adenomatous goiter (AG). Several ancillary markers have been suggested to aid in the diagnosis of FTC, but the successful use of these methods still needs to be validated. Methods: In the present study, we verified the immunoexpression of HMGA2, CEACAM6, survivin, and SFN/14-3-3 δ in lesions including 41 AGs, 72 FAs, and 79 FTCs. We evaluated their diagnostic usefulness, combined with galectin 3, Hector Battifora mesothelial 1 (HBME1), cytokeratin 19, and cyclin D1, in diagnosing FTC. Results: The expressions of HBME1 (65.8%) and HMGA2 (55.7%) were significantly higher in FTCs than in FAs and AGs (p<.001 and p=.005, respectively). HBME1 was the only marker that was more frequently expressed in FTCs than in FAs (p=.021) and it was more frequently expressed in follicular neoplasms than in AGs (p<.001). Among the novel markers, the combination of HMGA2 and HBME1 showed the highest sensitivity (72.2%) and specificity (76.1%) for diagnosing FTC. CEACAM6, survivin, and SFN/14-3-3 δ were barely expressed in most cases. Conclusions: Our present results show that only HMGA2 can be beneficial in differentiating FTC using the novel markers.

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HMGA2 promotes nasopharyngeal carcinoma progression and is associated with tumor resistance and poor prognosis
Xinting Ouyang, Kangxin Li, Jiaqi Wang, Weijian Zhu, Qiang Yi, Jinghua Zhong
Frontiers in Oncology.2024;[Epub] CrossRef
miR‐98‐5p promotes apoptosis and inhibits migration and cell growth in papillary thyroid carcinoma through Bax/Caspase‐3 by HMGA2
Kai Qiu, QingJi Xie, Shan Jiang, Ting Lin
Journal of Clinical Laboratory Analysis.2020;[Epub] CrossRef
High mobility group A protein-2 as a tumor cancer diagnostic and prognostic marker: a systematic review and meta-analysis
Yen Thi-Hai Pham, Ovie Utuama, Claire E. Thomas, Jong A. Park, Carlo La Vecchia, Harvey A. Risch, Chi Thi-Du Tran, Thanh V. Le, Paolo Boffetta, Leon Raskin, Hung N. Luu
European Journal of Cancer Prevention.2020; 29(6): 565. CrossRef
Diagnostic performance of HMGA2 gene expression for differentiation of malignant thyroid nodules: A systematic review and meta‐analysis
Bo Hyun Kim, Seong Jang Kim, Mijin Kim, Sang‐Woo Lee, Shin Young Jeong, Kyoungjune Pak, Keunyoung Kim, In Joo Kim
Clinical Endocrinology.2018; 89(6): 856. CrossRef
Thyroid follicular adenomas and carcinomas: molecular profiling provides evidence for a continuous evolution
Geneviève Dom, Sandra Frank, Sebastien Floor, Pashalina Kehagias, Frederick Libert, Catherine Hoang, Guy Andry, Alex Spinette, Ligia Craciun, Nicolas de Saint Aubin, Christophe Tresallet, Frederique Tissier, Frederique Savagner, Samira Majjaj, Ilse Gutier
Oncotarget.2018; 9(12): 10343. CrossRef
APLP2, RRM2, and PRC1: New Putative Markers for the Differential Diagnosis of Thyroid Follicular Lesions
Esmeralda Castelblanco, Carles Zafon, Javier Maravall, Pilar Gallel, Montserrat Martinez, Ismael Capel, Maria Rosa Bella, Irene Halperin, Jordi Temprana, Carmela Iglesias, Manel Puig-Domingo, Mercedes Robledo, Xavier Matias-Guiu, Didac Mauricio
Thyroid.2017; 27(1): 59. CrossRef
Prognostic implication of histological features associated with EHD2 expression in papillary thyroid carcinoma
Yourha Kim, Min-Hee Kim, Sora Jeon, Jeeyoon Kim, Chankyung Kim, Ja Seong Bae, Chan Kwon Jung, Yves St-Pierre
PLOS ONE.2017; 12(3): e0174737. CrossRef
Survivin DEx3 as a biomarker of thyroid cancers: A study at the mRNA and protein level
Joanna Waligórska-Stachura, Nadia Sawicka-Gutaj, Maciej Zabel, Mirosław Andrusiewicz, Paweł Gut, Agata Czarnywojtek, Marek Ruchała
Oncology Letters.2017; 13(4): 2437. CrossRef
High-Frequency Ultrasound-Guided Injection for the Generation of a Novel Orthotopic Mouse Model of Human Thyroid Carcinoma
Adelaide Greco, Sandra Albanese, Luigi Auletta, Peppino Mirabelli, Antonella Zannetti, Crescenzo D'Alterio, Gennaro Di Maro, Francesca Maria Orlandella, Giuliana Salvatore, Andrea Soricelli, Marco Salvatore
Thyroid.2016; 26(4): 552. CrossRef
The study of galectin-3, Ki-67, ubiquitin, HMGA-2 by polymerase chain reaction in real time (RT-PCR) in the puncture specimens of nodular goiter
Irina S. Berjozkina, Tat'jana V. Saprina, Anastasija P. Zima, Anna V. Isaeva, Venera N. Latipova, Marat R. Muhamedov, Leonid R. Bazilevich, Oleg S. Popov, Dar'ja A. Skuratovskaja, Kristina A. Jurova, Larisa C. Litvinova
Clinical and experimental thyroidology.2016; 12(2): 19. CrossRef
High-mobility group A2 overexpression is an unfavorable prognostic biomarker for nasopharyngeal carcinoma patients
Zhuoxing Liu, Kunpeng Wu, Zhixiong Yang, Aibing Wu
Molecular and Cellular Biochemistry.2015; 409(1-2): 155. CrossRef
Defining the value of CD56, CK19, Galectin 3 and HBME-1 in diagnosis of follicular cell derived lesions of thyroid with systematic review of literature
Duško Dunđerović, Jasmina Marković Lipkovski, Ivan Boričic, Ivan Soldatović, Vesna Božic, Dubravka Cvejić, Svetislav Tatić
Diagnostic Pathology.2015;[Epub] CrossRef

Fine Needle Aspiration Cytology of Thyroid Follicular Neoplasm: Cytohistologic Correlation and Accuracy: Changyoung Yoo, Hyun Joo Choi, Soyoung Im, Ji Han Jung, Kiouk Min, Chang Suk Kang, Young-Jin Suh; Korean J Pathol. 2013;47(1):61-66. Published online February 25, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.1.61

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Abstract PDF

Background

This study evaluated the accuracy of fine needle aspiration cytology (FNAC) in cases of follicular neoplasm (FN) on the basis of histologic diagnosis, and reviewed the cytologic findings of FN according to the FNAC.

Methods

Among the 66 cases diagnosed with thyroid FN by FNAC during the 7-year period from 2003 to 2009, 36 cases that had undergone thyroid surgery were available for review. Cytologic diagnosis was compared with the histologic diagnosis of each case.

Results

Among the 36 cases with a cytologic diagnosis of thyroid FN, histologic diagnosis was as follows: 20 follicular adenomas (55.6%), 3 Hurthle cell adenomas (8.3%), 2 follicular carcinomas (5.6%), 8 nodular goiters (22.2%), 2 papillary carcinomas (5.6%), and 1 Hashimoto's thyroiditis (2.8%), resulting in a diagnostic accuracy of FNAC for thyroid FN of 69.5%.

Conclusions

This study shows that FNAC for thyroid FN is a useful primary screening method because when FN is diagnosed by FNAC, the rate of FN histologic diagnosis is relatively high, however, adequate sampling and experience is a prerequisite for this procedure.

Citations

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Prevalence and Predictors of Malignancy in Contralateral Thyroid Lobe in Patients Undergoing Completion Thyroidectomy
Pradipta Kumar Parida, Siddhartha Pradhan, Chapity Preetam, Pradeep Pradhan, Dillip Kumar Samal, Saurav Sarkar
Indian Journal of Otolaryngology and Head & Neck Surgery.2022; 74(S2): 2053. CrossRef
Ultrasonographic and cytologic assessments of follicular neoplasms of the thyroid: Predictive features differentiating follicular carcinoma from follicular adenoma
Hye Shin Ahn, Hee Sung Kim, Min Ji Hong, Paula Soares
PLOS ONE.2022; 17(7): e0271437. CrossRef
2019 Practice guidelines for thyroid core needle biopsy: a report of the Clinical Practice Guidelines Development Committee of the Korean Thyroid Association
Chan Kwon Jung, Jung Hwan Baek, Dong Gyu Na, Young Lyun Oh, Ka Hee Yi, Ho-Cheol Kang
Journal of Pathology and Translational Medicine.2020; 54(1): 64. CrossRef
Preoperative diagnostic categories of fine needle aspiration cytology for histologically proven thyroid follicular adenoma and carcinoma, and Hurthle cell adenoma and carcinoma: Analysis of cause of under- or misdiagnoses
Hee Young Na, Jae Hoon Moon, June Young Choi, Hyeong Won Yu, Woo-Jin Jeong, Yeo Koon Kim, Ji-Young Choe, So Yeon Park, Paula Soares
PLOS ONE.2020; 15(11): e0241597. CrossRef
Core needle biopsy of thyroid nodules: outcomes and safety from a large single-center single-operator study
Jooae Choe, Jung Hwan Baek, Hye Sun Park, Young Jun Choi, Jeong Hyun Lee
Acta Radiologica.2018; 59(8): 924. CrossRef
Cytological Features That Differentiate Follicular Neoplasm from Mimicking Lesions
Kanghee Han, Hwa-Jeong Ha, Joon Seog Kong, Jung-Soon Kim, Jae Kyung Myung, Jae Soo Koh, Sunhoo Park, Myung-Soon Shin, Woo-Tack Song, Hye Sil Seol, Seung-Sook Lee
Journal of Pathology and Translational Medicine.2018; 52(2): 110. CrossRef
Comparison of the Diagnostic Efficacy of Ultrasound‐Guided Core Needle Biopsy With 18‐ Versus 20‐Gauge Needles for Thyroid Nodules
Hye Shin Ahn, Mirinae Seo, Su Min Ha, Hee Sung Kim
Journal of Ultrasound in Medicine.2018; 37(11): 2565. CrossRef
Subclassification of Bethesda Atypical and Follicular Neoplasm Categories According to Nuclear and Architectural Atypia Improves Discrimination of Thyroid Malignancy Risk
Joel Xue Yi Lim, Min En Nga, Dedrick Kok Hong Chan, Wee Boon Tan, Rajeev Parameswaran, Kee Yuan Ngiam
Thyroid.2018; 28(4): 511. CrossRef
The expression profile of integrin receptors and osteopontin in thyroid malignancies varies depending on the tumor progression rate and presence of BRAF V600E mutation
Galina Chernaya, Nina Mikhno, Tatiana Khabalova, Svetlana Svyatchenko, Lyudmila Mostovich, Sergey Shevchenko, Lyudmila Gulyaeva
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The Usefulness of Immunocytochemistry of CD56 in Determining Malignancy from Indeterminate Thyroid Fine-Needle Aspiration Cytology
Hyunseo Cha, Ju Yeon Pyo, Soon Won Hong
Journal of Pathology and Translational Medicine.2018; 52(6): 404. CrossRef
Core Needle Biopsy of the Thyroid: 2016 Consensus Statement and Recommendations from Korean Society of Thyroid Radiology
Dong Gyu Na, Jung Hwan Baek, So Lyung Jung, Ji-hoon Kim, Jin Yong Sung, Kyu Sun Kim, Jeong Hyun Lee, Jung Hee Shin, Yoon Jung Choi, Eun Ju Ha, Hyun Kyung Lim, Soo Jin Kim, Soo Yeon Hahn, Kwang Hwi Lee, Young Jun Choi, Inyoung Youn, Young Joong Kim, Hye Sh
Korean Journal of Radiology.2017; 18(1): 217. CrossRef
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Su Min Ha, Jin Yong Sung, Jung Hwan Baek, Dong Gyu Na, Ji-hoon Kim, Hyunju Yoo, Ducky Lee, Dong Whan Choi
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Ja-Seong Bae, Seung Kyu Choi, Sora Jeon, Yourha Kim, Sohee Lee, Youn Soo Lee, Chan Kwon Jung
International Journal of Endocrinology.2014; 2014: 1. CrossRef
Diagnosis of Thyroid Follicular Neoplasm: Fine-Needle Aspiration Versus Core-Needle Biopsy
Ra Gyoung Yoon, Jung Hwan Baek, Jeong Hyun Lee, Young Jun Choi, Min Ji Hong, Dong Eun Song, Jae Kyun Kim, Jong Ho Yoon, Won Bae Kim
Thyroid.2014; 24(11): 1612. CrossRef

Morphometric Study on Fine Needle Aspirates from Follicular Adenoma and Follicular Carcinoma of the Thyroid.: Young Chae Chu, Hee Jung Cha, Soo Kee Min, Joon Mee Kim, Tae Sook Hwang; Korean J Cytopathol. 1998;9(1):63-68.

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Abstract PDF: Fine needle aspiration cytology of "cold" nodules of the thyroid has proved to be of great value in their preoperative diagnosis. Most types of thyroid tumors are readily recognizable from characteristic cellular patterns in the smears of needle aspirates. But follicular neoplasms present some problems because the cytomorphology of the adenomas frequently is same as in carcinoma. For differentiation of benign from malignant follicular neoplasms of the thyroid we tested the usefulness of two objective parameters - nuclear area and perimeter - by morphometry. This study was made on fine needle aspirates from 30 cases with cytologic diagnosis of follicular neoplasm of thyroid. The histologic classification was follicular adenoma in 22 cases and follicular carcinoma in 8 cases. As a reference group we used seven caes with nodular hyperplasia. The smears of aspirates were stained by Papanicolaou method. On each slide 200 randomly selected cells with intact nuclei were measured. The mean value of nuclear area are 25.32+/-5.50 micrometer2, 34.08+/-7.50 micrometer2 and 39.97+/-6.63 micrometer2 in nodular hyperplasia, follicular adenoma, and follicular carcinoma, respectively. The mean value of perimeter are 19.48+/-2.26 micrometer, 22.95+/-2.65 micrometer and 24.78+/-2.23 micrometer in nodular hyperplasia, follicular adenoma and follicular carcinoma, respectively. The mean nuclear areas and perimeters of cells from follicular adenoma were significantly larger than those from nodular hyperplasia (p<0.05). The mean nuclear areas and perimeters of cells from follicular carcinoma were larger than those from follicular adenoma but the differences are not significant statistically(p<0.05). Therefore, morphometric assessment alone is inadequate to predict malignancy in thyroid aspirates.

A Study on the Cytologic Features of Fine Needle Aspiration Cytology in the Thyroid Follicular Neoplasm and Nodular Goiter.: Jin Ye Yoo, Hye Jae Cho, Il Hyang Ko; Korean J Cytopathol. 1998;9(1):69-78.

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Abstract PDF: There is a lot of difficulty in the diagnosis of follicular lesions of the thyroid by fine needle aspiration cytology(FNAC). The main purpose of this report is offering more guidance regarding the cytologic appearance to distinguish follicular neoplasm from nodular goiter and laying stress on the presence of mixed group. The histologic and cytologic findings of 23 follicular neoplasms and 13 nodular (adenomatous) goiters were reviewed. Histologic specimens were classified into the microfollicular(MIF), mixed(MIX), and nodular goiter(NG) groups. The comparison of histologic patterns with histologic diagnosis revealed that all the lesions with predominantly microfollicular, trabecular, or solid pattern were follicular carcinoma and all the lesions with predominantly macrofollicular pattern were nodular goiter. The distinguishing cytologic features for the MIF group were irregular cell arrangement in cell groups(100%, p=0.00001), absence of atrophic follicular cells(100%, p=0.0007), abundant microfollicles(100%, p=0.002), pleomorphic nuclei(100%, p=0.002), not predominant syncytial smear pattern(100%, p=0.002), heterochromatin(100%, p=0.032), absence of macrofollicles(100%, p=0.038), scant colloid(100%, p=0.04), clear background(83%, p=0.00006), and uniform sized follicles(83%, p=0.014). And regular cell arrangement(honeycomb appearance) in cell groups(85%, p=0.0000), atrophic change of follicular cells(69%, p=0.0002), syncytial smear pattern(54%, p=0.006), monomorphic nuclei(85%, p=0.008), and hemorrhagic background(100%, p=0.027) were characteristic features of the NG group. Seventeen out of 36 cases(47%) were the MIX group composed of combined cytologic features of the MIF and NG groups. Therefore the frequent presence of the MIX group is considered to be main cause of the difficultyin the diagnosis of follicular lesions by FNAC. The mixed morphologic feature may support the hypothesis of a biologic "continuum" between nodular goiter and follicular neoplasm of thyroid gland.

Case Report

Fine Needle Aspiration Cytology of Parathyroid Neoplasms: A Review of Three Cases.: Lucia Kim, Jee Young Han, In Suh Park, Suk Jin Choi, Joon Mee Kim, Young Chae Chu; Korean J Cytopathol. 2007;18(1):74-80.

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Abstract PDF: Parathyroid tumors may be difficult to distinguish from thyroid follicular lesions, especially when a tumor is nonfunctioning. We report here two cases of asymptomatic parathyroid carcinoma preoperatively misdiagnosed as thyroid follicular lesions, and one case of parathyroid adenoma showing hyperparathyroidism, and review the cytologic features favoring the diagnosis of parathyroid neoplasm. The cytologic findings that are characterized by clean background, monomorphic small cells, cohesive three-dimensional papillary clusters, small tight clusters with scattered naked nuclei, and well-defined clear cytoplasm favor a diagnosis for the parathyroid lesions. Cytologic findings such as macrofollicular structure, presence of colloid and macrophages, and presence of perivacuolar cytoplasmic granules on May-Grunwald-Giemsa stain support a diagnosis of a thyroid follicular lesion. The cytomorphology of parathyroid tumors is so variable that the distinction from a thyroid lesion cannot be based on the presence or absence of a single feature only but on the cytologic features as a whole.

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