Journal of Pathology and Translational Medicine

Ju Yeon Pyo

6 Articles

A Multi-institutional Study of Prevalence and Clinicopathologic Features of Non-invasive Follicular Thyroid Neoplasm with Papillary-like Nuclear Features (NIFTP) in Korea: Ja Yeong Seo, Ji Hyun Park, Ju Yeon Pyo, Yoon Jin Cha, Chan Kwon Jung, Dong Eun Song, Jeong Ja Kwak, So Yeon Park, Hee Young Na, Jang-Hee Kim, Jae Yeon Seok, Hee Sung Kim, Soon Won Hong; J Pathol Transl Med. 2019;53(6):378-385. Published online October 21, 2019; DOI: https://doi.org/10.4132/jptm.2019.09.18

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Background
In the present multi-institutional study, the prevalence and clinicopathologic characteristics of non-invasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) were evaluated among Korean patients who underwent thyroidectomy for papillary thyroid carcinoma (PTC).
Methods
Data from 18,819 patients with PTC from eight university hospitals between January 2012 and February 2018 were retrospectively evaluated. Pathology reports of all PTCs and slides of potential NIFTP cases were reviewed. The strict criterion of no papillae was applied for the diagnosis of NIFTP. Due to assumptions regarding misclassification of NIFTP as non-PTC tumors, the lower boundary of NIFTP prevalence among PTCs was estimated. Mutational analysis for BRAF and three RAS isoforms was performed in 27 randomly selected NIFTP cases.
Results
The prevalence of NIFTP was 1.3% (238/18,819) of all PTCs when the same histologic criteria were applied for NIFTP regardless of the tumor size but decreased to 0.8% (152/18,819) when tumors ≥1 cm in size were included. The mean follow-up was 37.7 months and no patient with NIFTP had evidence of lymph node metastasis, distant metastasis, or disease recurrence during the follow-up period. A difference in prevalence of NIFTP before and after NIFTP introduction was not observed. BRAF^V600E mutation was not found in NIFTP. The mutation rate for the three RAS genes was 55.6% (15/27).
Conclusions
The low prevalence and indolent clinical outcome of NIFTP in Korea was confirmed using the largest number of cases to date. The introduction of NIFTP may have a small overall impact in Korean practice.

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Analysis of a pre-2017 follicular variant papillary thyroid carcinoma cohort reclassified as noninvasive follicular thyroid neoplasm with papillary-like features (NIFTP): an 11-year retrospective single institution experience
Shaham Beg, Sana Irfan Khan, Isabella Cui, Theresa Scognamiglio, Rema Rao
Journal of the American Society of Cytopathology.2023; 12(2): 112. CrossRef
Noninvasive Follicular Thyroid Neoplasm With Papillary-Like Nuclear Features: What a Surgeon Should Know
Jabir Alharbi, Thamer Alraddadi, Haneen Sebeih, Mohammad A Alessa, Haddad H Alkaf, Ahmed Bahaj, Sherif K Abdelmonim
Cureus.2023;[Epub] CrossRef
NTRK Fusion in a Cohort of BRAF p. V600E Wild-Type Papillary Thyroid Carcinomas
Seung Eun Lee, Mi-Sook Lee, Heejin Bang, Mi Young Kim, Yoon-La Choi, Young Lyun Oh
Modern Pathology.2023; 36(8): 100180. CrossRef
A Comprehensive Study on the Diagnosis and Management of Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features
Bayan A. Alzumaili, Lauren N. Krumeich, Reagan Collins, Timothy Kravchenko, Emad I. Ababneh, Adam S. Fisch, William C. Faquin, Vania Nosé, Maria Martinez-Lage, Gregory W. Randolph, Rajshri M. Gartland, Carrie C. Lubitz, Peter M. Sadow
Thyroid.2023; 33(5): 566. CrossRef
Clinical-Pathological and Molecular Evaluation of 451 NIFTP Patients from a Single Referral Center
Paola Vignali, Agnese Proietti, Elisabetta Macerola, Anello Marcello Poma, Liborio Torregrossa, Clara Ugolini, Alessio Basolo, Antonio Matrone, Teresa Rago, Ferruccio Santini, Rossella Elisei, Gabriele Materazzi, Fulvio Basolo
Cancers.2022; 14(2): 420. CrossRef
Noninvasive follicular thyroid neoplasm with papillary-like nuclear features: its updated diagnostic criteria, preoperative cytologic diagnoses and impact on the risk of malignancy
Hee Young Na, So Yeon Park
Journal of Pathology and Translational Medicine.2022; 56(6): 319. CrossRef
SFE-AFCE-SFMN 2022 Consensus on the management of thyroid nodules : Follow-up: How and how long?
Sophie Leboulleux, Livia Lamartina, Emmanuelle Lecornet Sokol, Fabrice Menegaux, Laurence Leenhardt, Gilles Russ
Annales d'Endocrinologie.2022; 83(6): 407. CrossRef
Different Threshold of Malignancy for RAS-like Thyroid Tumors Causes Significant Differences in Thyroid Nodule Practice
Kennichi Kakudo
Cancers.2022; 14(3): 812. CrossRef
Clinicopathological parameters for predicting non-invasive follicular thyroid neoplasm with papillary features (NIFTP)
Eunju Jang, Kwangsoon Kim, Chan Kwon Jung, Ja Seong Bae, Jeong Soo Kim
Therapeutic Advances in Endocrinology and Metabolism.2021; 12: 204201882110005. CrossRef
The Incidence of Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features: A Meta-Analysis Assessing Worldwide Impact of the Reclassification
Chanchal Rana, Huy Gia Vuong, Thu Quynh Nguyen, Hoang Cong Nguyen, Chan Kwon Jung, Kennichi Kakudo, Andrey Bychkov
Thyroid.2021;[Epub] CrossRef
The Genomic Landscape of Thyroid Cancer Tumourigenesis and Implications for Immunotherapy
Amandeep Singh, Jeehoon Ham, Joseph William Po, Navin Niles, Tara Roberts, Cheok Soon Lee
Cells.2021; 10(5): 1082. CrossRef
Noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) is rare, benign lesion using modified stringent diagnostic criteria: Reclassification and outcome study
David Cubero Rego, Hwajeong Lee, Anne Boguniewicz, Timothy A. Jennings
Annals of Diagnostic Pathology.2020; 44: 151439. CrossRef
Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features: From Echography to Genetic Profile
Francesca Maletta, Enrico Costantino Falco, Alessandro Gambella, Jasna Metovic, Mauro Papotti
The Tohoku Journal of Experimental Medicine.2020; 252(3): 209. CrossRef

The Usefulness of Immunocytochemistry of CD56 in Determining Malignancy from Indeterminate Thyroid Fine-Needle Aspiration Cytology: Hyunseo Cha, Ju Yeon Pyo, Soon Won Hong; J Pathol Transl Med. 2018;52(6):404-410. Published online October 15, 2018; DOI: https://doi.org/10.4132/jptm.2018.09.20

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Abstract PDF

Background
Fine-needle aspiration cytology serves as a safe, economical tool in evaluating thyroid nodules. However, about 30% of the samples are categorized as indeterminate. Hence, many immunocytochemistry markers have been studied, but there has not been a single outstanding marker. We studied the efficacy of CD56 with human bone marrow endothelial cell marker-1 (HBME-1) in diagnosis in the Bethesda System for Reporting Thyroid Cytopathology (TBSRTC) category III.
Methods
We reviewed ThinPrep liquid-based cytology (LBC) samples with Papanicolaou stain from July 1 to December 31, 2016 (2,195 cases) and selected TBSRTC category III cases (n = 363). Twenty-six cases were histologically confirmed as benign (six cases, 23%) or malignant (20 cases, 77%); we stained 26 LBC slides with HBME-1 and CD56 through the cell transfer method. For evaluation of reactivity of immunocytochemistry, we chose atypical follicular cell clusters.
Results
CD56 was not reactive in 18 of 20 cases (90%) of malignant nodules and showed cytoplasmic positivity in five of six cases (83%) of benign nodules. CD56 showed high sensitivity (90.0%) and relatively low specificity (83.3%) in detecting malignancy (p = .004). HBME-1 was reactive in 17 of 20 cases (85%) of malignant nodules and was not reactive in five of six cases (83%) of benign nodules. HBME-1 showed slightly lower sensitivity (85.0%) than CD56. The specificity in detecting malignancy by HBME-1 was similar to that of CD56 (83.3%, p = .008). CD56 and HBME-1 tests combined showed lower sensitivity (75.0% vs 90%) and higher specificity (93.8% vs 83.3%) in detecting malignancy compared to using CD56 alone.
Conclusions
Using CD56 alone showed relatively low specificity despite high sensitivity for detecting malignancy. Combining CD56 with HBME-1 could increase the specificity. Thus, we suggest that CD56 could be a useful preoperative marker for differential diagnosis of TBSRTC category III samples.

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Preoperative evaluation of thyroid nodules – Diagnosis and management strategies
Tapoi Dana Antonia, Lambrescu Ioana Maria, Gheorghisan-Galateanu Ancuta-Augustina
Pathology - Research and Practice.2023; 246: 154516. CrossRef
Immunocytochemistry in thyroid cytology and its multiple roles: a systematic review
Federica Policardo, Pietro Tralongo, Angela Feraco, Federica Vegni, Angela Carlino, Alfredo Pontecorvi, Celestino Pio Lombardi, Marco Raffaelli, Francesco Pierconti, Luigi Maria Larocca, Esther Diana Rossi
Diagnostic Histopathology.2023; 29(8): 386. CrossRef
Paving the path toward multi-omics approaches in the diagnostic challenges faced in thyroid pathology
Isabella Piga, Vincenzo L’Imperio, Giulia Capitoli, Vanna Denti, Andrew Smith, Fulvio Magni, Fabio Pagni
Expert Review of Proteomics.2023; 20(12): 419. CrossRef
CD56 Expression in Papillary Thyroid Carcinoma Is Highly Dependent on the Histologic Subtype: A Potential Diagnostic Pitfall
Uiju Cho, Yourha Kim, Sora Jeon, Chan Kwon Jung
Applied Immunohistochemistry & Molecular Morphology.2022; 30(5): 389. CrossRef

Preoperative Cytologic Diagnosis of Warthin-like Variant of Papillary Thyroid Carcinoma: Jisup Kim, Beom Jin Lim, Soon Won Hong, Ju Yeon Pyo; J Pathol Transl Med. 2018;52(2):105-109. Published online February 12, 2018; DOI: https://doi.org/10.4132/jptm.2017.12.26

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Abstract PDF

Background
Warthin-like variant of papillary thyroid carcinoma (WLV-PTC) is a relatively rare variant of papillary thyroid carcinoma with favorable prognosis. However, preoperative diagnosis using fine-needle aspiration (FNA) specimens is challenging especially with lymphocytic thyroiditis characterized by Hürthle cells and lymphocytic background. To determine a helpful cytological differential point, we compared WLV-PTC FNA findings with conventional papillary thyroid carcinoma with lymphocytic thyroiditis (PTC-LT) and conventional papillary thyroid carcinoma without lymphocytic thyroiditis (PTC) regarding infiltrating inflammatory cells and their distribution. Preoperative diagnosis or potential for WLV-PTC will be helpful for surgeons to decide the scope of operation.
Methods
Of the 8,179 patients treated for papillary thyroid carcinoma between January 2007 and December 2012, 16 patients (0.2%) were pathologically confirmed as WLV-PTC and four cases were available for cytologic review. For comparison, we randomly selected six PTC-LT cases and five PTC cases during the same period. The number of intratumoral and background lymphocytes, histiocytes, neutrophils, and the presence of giant cells were evaluated and compared using conventional smear and ThinPrep preparations.
Results
WLV-PTC showed extensive lymphocytic smear with incorporation of thyroid follicular tumor cell clusters and frequent histiocytes. WLV-PTC was associated with higher intratumoral and background lymphocytes and histiocytes compared with PTC-LT or PTC. The difference was more distinct in liquid-based cytology.
Conclusions
The lymphocytic smear pattern and the number of inflammatory cells of WLV-PTC are different from those of PTC-LT or PTC and will be helpful for the differential diagnosis of WLV-PTC in preoperative FNA.

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Warthin-like variant of papillary thyroid carcinoma with lymph node metastases: a case report and review of the literature
Andrii Hryshchyshyn, Andrii Bahrii, Pavlina Botsun, Volodymyr Chuba
Journal of Medical Case Reports.2024;[Epub] CrossRef
Warthin-like papillary thyroid carcinoma: a case report and comprehensive review of the literature
Abdel Mouhaymen Missaoui, Fatma Hamza, Wafa Belabed, Manel Mellouli, Mohamed Maaloul, Slim Charfi, Issam Jardak, Tahya Sellami-Boudawara, Nabila Rekik, Mohamed Abid
Frontiers in Endocrinology.2023;[Epub] CrossRef
The Warthin-like variant of papillary thyroid carcinomas: a clinicopathologic analysis report of two cases
Xing Zhao, Yijia Zhang, Pengyu Hao, Mingzhen Zhao, Xingbin Shen
Oncologie.2023; 25(5): 581. CrossRef
Challenges in Cytology Specimens With Hürthle Cells
Eleni Thodou, Sule Canberk, Fernando Schmitt
Frontiers in Endocrinology.2021;[Epub] CrossRef
Warthin-like variant of Papillary thyroid carcinoma—Case report of an uncommon tumour with review of literature
Pradyumna Kumar Sahoo, Rashmi Patnayak, Perwez Alam Khan, Amitabh Jena
International Journal of Surgery Case Reports.2020; 77: 9. CrossRef

Thyroid Fine-Needle Aspiration Cytology Practice in Korea: Yoon Jin Cha, Ju Yeon Pyo, SoonWon Hong, Jae Yeon Seok, Kyung-Ju Kim, Jee-Young Han, Jeong Mo Bae, Hyeong Ju Kwon, Yeejeong Kim, Kyueng-Whan Min, Soonae Oak, Sunhee Chang; J Pathol Transl Med. 2017;51(6):521-527. Published online October 11, 2017; DOI: https://doi.org/10.4132/jptm.2017.09.26

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Abstract PDF

We reviewed the current status of thyroid fine-needle aspiration cytology (FNAC) in Korea. Thyroid aspiration biopsy was first introduced in Korea in 1977. Currently, radiologists aspirate the thyroid nodule under the guidance of ultrasonography, and cytologic interpretation is only legally approved when a cytopathologist makes the diagnosis. In 2008, eight thyroid-related societies came together to form the Korean Thyroid Association. The Korean Society for Cytopathology and the endocrine pathology study group of the Korean Society for Pathologists have been updating the cytologic diagnostic guidelines. The Bethesda System for Reporting Thyroid Cytopathology was first introduced in 2009, and has been used by up to 94% of institutions by 2016. The average diagnosis rates are as follows for each category: I (12.4%), II (57.9%), III (10.4%), IV (2.9%), V (3.7%), and VI (12.7%). The malignancy rates in surgical cases are as follows for each category: I (28.7%), II (27.8%), III (50.6%), IV (52.3%), V (90.7%), and VI (100.0%). Liquid-based cytology has been used since 2010, and it was utilized by 68% of institutions in 2016. The categorization of thyroid lesions into “atypia of undetermined significance” or “follicular lesion of undetermined significance” is necessary to draw consensus in our society. Immunocytochemistry for galectin-3 and BRAF is used. Additionally, a molecular test for BRAF in thyroid FNACs is actively used. Core biopsies were performed in only 44% of institutions. Even the institutions that perform core biopsies only perform them for less than 3% of all FNACs. However, only 5% of institutions performed core biopsies up to three times more than FNAC.

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State of the art of thyroid pathology: FNA diagnostic accuracy in an intermediate center in Ibagué
Daniel Javier Velez Bohorquez, Nohora Bibiana Varon Arce, Sandra Milena Tellez Olaya, Sebastian Camilo Mora Garcia, Anggi Margarita Velez Bohorquez, Mabel Elena Bohorquez Lozano
Universitas Médica.2023;[Epub] CrossRef
The Asian Thyroid Working Group, from 2017 to 2023
Kennichi Kakudo, Chan Kwon Jung, Zhiyan Liu, Mitsuyoshi Hirokawa, Andrey Bychkov, Huy Gia Vuong, Somboon Keelawat, Radhika Srinivasan, Jen-Fan Hang, Chiung-Ru Lai
Journal of Pathology and Translational Medicine.2023; 57(6): 289. CrossRef
Diagnostic value of thyroid imaging reporting and data system combined with BRAFV600E mutation analysis in Bethesda categories III–V thyroid nodules
Liuxi Wu, Hua Shu, Wenqin Chen, Yingqian Gao, Ya Yuan, Xiao Li, Wenjuan Lu, Xinhua Ye, Hongyan Deng
Scientific Reports.2022;[Epub] CrossRef
Contribution of cytologic examination to diagnosis of poorly differentiated thyroid carcinoma
Na Rae Kim, Jae Yeon Seok, Yoo Seung Chung, Joon Hyop Lee, Dong Hae Chung
Journal of Pathology and Translational Medicine.2020; 54(2): 171. CrossRef
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Adrien Ben Hamou, Stéphanie Espiard, Christine Do Cao, Miriam Ladsous, Camille Loyer, Alexandre Moerman, Samuel Boury, Maéva Kyheng, Claire-Marie Dhaenens, Vincent Tiffreau, Pascal Pigny, Gilles Lebuffe, Robert Caiazzo, Sébastien Aubert, Marie Christine V
Orphanet Journal of Rare Diseases.2019;[Epub] CrossRef
The History of Korean Thyroid Pathology
Soon Won Hong, Chan Kwon Jung
International Journal of Thyroidology.2018; 11(1): 15. CrossRef
BRAFV600E Mutation is a Strong Preoperative Indicator for Predicting Malignancy in Thyroid Nodule Patients with Atypia of Undetermined Significance Identified by Fine Needle Aspiration
Hye Rang Choi, Bo-Yoon Choi, Jae Hoon Cho, Young Chang Lim
Korean Journal of Otorhinolaryngology-Head and Neck Surgery.2018; 61(11): 600. CrossRef
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
Thyroid FNA cytology in Asian practice—Active surveillance for indeterminate thyroid nodules reduces overtreatment of thyroid carcinomas
K. Kakudo, M. Higuchi, M. Hirokawa, S. Satoh, C. K. Jung, A. Bychkov
Cytopathology.2017; 28(6): 455. CrossRef
The Use of Fine-Needle Aspiration (FNA) Cytology in Patients with Thyroid Nodules in Asia: A Brief Overview of Studies from the Working Group of Asian Thyroid FNA Cytology
Chan Kwon Jung, SoonWon Hong, Andrey Bychkov, Kennichi Kakudo
Journal of Pathology and Translational Medicine.2017; 51(6): 571. CrossRef

The Intraoperative Immunohistochemical Staining of CD56 and CK19 Improves Surgical Decision for Thyroid Follicular Lesions: Ju Yeon Pyo, Sung-eun Choi, Eunah Shin, JaSeung Koo, SoonWon Hong; J Pathol Transl Med. 2017;51(5):463-470. Published online August 2, 2017; DOI: https://doi.org/10.4132/jptm.2017.05.25

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Abstract PDF

Background
When differential diagnosis is difficult in thyroid follicular lesions with overlapping histological features, the immunohistochemical staining can help confirm the diagnosis. We aimed to evaluate the effectiveness of rapid immunohistochemical stains of CD56 and cytokeratin 19 on frozen sections of thyroid follicular lesion and explore the possible gains and limitations of the practice. Methods: Eighty-six nodules of 79 patients whose intraoperative frozen sections were selected as the control group, and 53 nodules of 48 patients whose intraoperative frozen sections were subject to rapid immunohistochemistry were selected as the study group. Results: Five nodules (6%) in the control group were diagnosed as follicular neoplasm and six nodules (7%) were deferred. In the study group, six nodules (11%) were follicular neoplasm and none were deferred. Three nodules (4%) in the control group showed diagnostic discrepancy between the frozen and permanent diagnoses, but none in the study group. The average turnaround time for the frozen diagnosis of the control group was 24 minutes, whereas it was 54 minutes for the study group. Conclusions: Intraoperative rapid immunohistochemical stains significantly decreased the diagnostic discrepancy in this study. Considering the adverse effects of indefinite frozen diagnosis or discrepancy with permanent diagnoses, the intraoperative rapid immunohistochemical stain can help to accurately diagnose and hence provide guidance to surgical treatment.

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High-Contrast Facile Imaging with Target-Directing Fluorescent Molecular Rotors, the N3-Modified Thioflavin T Derivatives
Yuka Kataoka, Hiroto Fujita, Arina Afanaseva, Chioko Nagao, Kenji Mizuguchi, Yuuya Kasahara, Satoshi Obika, Masayasu Kuwahara
Biochemistry.2019; 58(6): 493. CrossRef
The diagnostic value of TROP-2, SLP-2 and CD56 expression in papillary thyroid carcinoma
Xueyang Yang, Yifang Hu, He Shi, Chengzhou Zhang, Zhixiao Wang, Xiaoyun Liu, Huanhuan Chen, Lijuan Zhang, Dai Cui
European Archives of Oto-Rhino-Laryngology.2018; 275(8): 2127. CrossRef

Clinicopathologic Correlations of E-cadherin and Prrx-1 Expression Loss in Hepatocellular Carcinoma: Kijong Yi, Hyunsung Kim, Yumin Chung, Hyein Ahn, Jongmin Sim, Young Chan Wi, Ju Yeon Pyo, Young-Soo Song, Seung Sam Paik, Young-Ha Oh; J Pathol Transl Med. 2016;50(5):327-336. Published online August 31, 2016; DOI: https://doi.org/10.4132/jptm.2016.06.22

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Abstract PDF

Background
Developing predictive markers for hepatocellular carcinoma (HCC) is important, because many patients experience recurrence and metastasis. Epithelial to mesenchymal transition (EMT) is a developmental process that plays an important role during embryogenesis and also during cancer metastasis. Paired-related homeobox protein 1 (Prrx-1) is an EMT inducer that has recently been introduced, and its prognostic significance in HCC is largely unknown.
Methods
Tissue microarray was constructed using surgically resected primary HCCs from 244 cases. Immunohistochemical staining of E-cadherin and Prrx-1 was performed. The correlation between E-cadherin loss and Prrx-1 expression, as well as other clinicopathologic factors, was evaluated.
Results
E-cadherin expression was decreased in 96 cases (39.4%). Loss of E-cadherin correlated with a higher recurrence rate (p < .001) but was not correlated with patient’s survival. Thirty-two cases (13.3%) showed at least focal nuclear Prrx-1 immunoreactivity while all non-neoplastic livers (n = 22) were negative. Prrx-1 expression was not associated with E-cadherin loss, survival or recurrence rates, pathologic factors, or the Ki-67 labeling index. Twenty tumors that were positive for E-cadherin and Prrx-1 had significantly higher nuclear grades than the rest of the cohort (p = .037). In Cox proportional hazard models, E-cadherin loss and large vessel invasion were independent prognostic factors for shorter disease-free survival. Cirrhosis and high Ki-67 index (> 40%) were independent prognostic factors for shorter overall survival.
Conclusions
Prrx-1 was expressed in small portions of HCCs but not in normal livers. Additional studies with a large number of Prrx-1-positive cases are required to confirm the results of this study.

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