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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
  • 6,488 View
  • 334 Download
  • 14 Web of Science
  • 14 Crossref
AbstractAbstract PDF
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. BRAFV600E 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.

Citations

Citations to this article as recorded by  
  • Case report & review: Bilateral NIFTP harboring concomitant HRAS and KRAS mutation: Report of an unusual case and literature review
    Marianna Rita Brogna, Francesca Collina, Maria Grazia Chiofalo, Debora De Bartolo, Angela Montone, Maria Rosaria Schiano, Michele Del Sesto, Nubia Pizza, Gerardo Ferrara
    Molecular Carcinogenesis.2024;[Epub]     CrossRef
  • 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 Use of the Bethesda System for Reporting Thyroid Cytopathology in Korea: A Nationwide Multicenter Survey by the Korean Society of Endocrine Pathologists
Mimi Kim, Hyo Jin Park, Hye Sook Min, Hyeong Ju Kwon, Chan Kwon Jung, Seoung Wan Chae, Hyun Ju Yoo, Yoo Duk Choi, Mi Ja Lee, Jeong Ja Kwak, Dong Eun Song, Dong Hoon Kim, Hye Kyung Lee, Ji Yeon Kim, Sook Hee Hong, Jang Sihn Sohn, Hyun Seung Lee, So Yeon Park, Soon Won Hong, Mi Kyung Shin
J Pathol Transl Med. 2017;51(4):410-417.   Published online June 14, 2017
DOI: https://doi.org/10.4132/jptm.2017.04.05
  • 9,163 View
  • 221 Download
  • 21 Web of Science
  • 20 Crossref
AbstractAbstract PDF
Background
The Bethesda System for Reporting Thyroid Cytopathology (TBSRTC) has standardized the reporting of thyroid cytology specimens. The objective of the current study was to evaluate the nationwide usage of TBSRTC and assess the malignancy rates in each category of TBSRTC in Korea.
Methods
Questionnaire surveys were used for data collection on the fine needle aspiration (FNA) of thyroid nodules at 74 institutes in 2012. The incidences and follow-up malignancy rates of each category diagnosed from January to December, 2011, in each institute were also collected and analyzed.
Results
Sixty out of 74 institutes answering the surveys reported the results of thyroid FNA in accordance with TBSRTC. The average malignancy rates for resected cases in 15 institutes were as follows: nondiagnostic, 45.6%; benign, 16.5%; atypical of undetermined significance, 68.8%; suspicious for follicular neoplasm (SFN), 30.2%; suspicious for malignancy, 97.5%; malignancy, 99.7%.
Conclusions
More than 80% of Korean institutes were using TBSRTC as of 2012. All malignancy rates other than the SFN and malignancy categories were higher than those reported by other countries. Therefore, the guidelines for treating patients with thyroid nodules in Korea should be revisited based on the malignancy rates reported in this study.

Citations

Citations to this article as recorded by  
  • Improved Diagnostic Accuracy of Thyroid Fine-Needle Aspiration Cytology with Artificial Intelligence Technology
    Yujin Lee, Mohammad Rizwan Alam, Hongsik Park, Kwangil Yim, Kyung Jin Seo, Gisu Hwang, Dahyeon Kim, Yeonsoo Chung, Gyungyub Gong, Nam Hoon Cho, Chong Woo Yoo, Yosep Chong, Hyun Joo Choi
    Thyroid®.2024; 34(6): 723.     CrossRef
  • Welcoming the new, revisiting the old: a brief glance at cytopathology reporting systems for lung, pancreas, and thyroid
    Rita Luis, Balamurugan Thirunavukkarasu, Deepali Jain, Sule Canberk
    Journal of Pathology and Translational Medicine.2024; 58(4): 165.     CrossRef
  • Predictors of Malignancy in Thyroid Nodules Classified as Bethesda Category III
    Xiaoli Liu, Jingjing Wang, Wei Du, Liyuan Dai, Qigen Fang
    Frontiers in Endocrinology.2022;[Epub]     CrossRef
  • Risk stratification of indeterminate thyroid nodules by novel multigene testing: a study of Asians with a high risk of malignancy
    Chunfang Hu, Weiwei Jing, Qing Chang, Zhihui Zhang, Zhenrong Liu, Jian Cao, Linlin Zhao, Yue Sun, Cong Wang, Huan Zhao, Ting Xiao, Huiqin Guo
    Molecular Oncology.2022; 16(8): 1680.     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
  • Malignancy rates in thyroid nodules: a long-term cohort study of 17,592 patients
    M Grussendorf, I Ruschenburg, G Brabant
    European Thyroid Journal.2022;[Epub]     CrossRef
  • Subclassification of the Bethesda Category III (AUS/FLUS): A study of thyroid FNA cytology based on ThinPrep slides from the National Cancer Center in China
    Huan Zhao, HuiQin Guo, LinLin Zhao, Jian Cao, Yue Sun, Cong Wang, ZhiHui Zhang
    Cancer Cytopathology.2021; 129(8): 642.     CrossRef
  • Effect of the Noninvasive Follicular Thyroid Neoplasm With Papillary-Like Nuclear Features (NIFTP) Nomenclature Revision on Indian Thyroid Fine-Needle Aspiration Practice
    Chanchal Rana, Pooja Ramakant, Divya Goel, Akanksha Singh, KulRanjan Singh, Suresh Babu, Anand Mishra
    American Journal of Clinical Pathology.2021; 156(2): 320.     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
  • Differences in surgical resection rate and risk of malignancy in thyroid cytopathology practice between Western and Asian countries: A systematic review and meta‐analysis
    Huy Gia Vuong, Hanh Thi Tuyet Ngo, Andrey Bychkov, Chan Kwon Jung, Trang Huyen Vu, Kim Bach Lu, Kennichi Kakudo, Tetsuo Kondo
    Cancer Cytopathology.2020; 128(4): 238.     CrossRef
  • Thyroid cancer among patients with thyroid nodules in Yemen: a three-year retrospective study in a tertiary center and a specialty clinic
    Butheinah A. Al-Sharafi, Jamila A. AlSanabani, Ibraheem M. Alboany, Amani M. Shamsher
    Thyroid Research.2020;[Epub]     CrossRef
  • Is Bethesda classification sufficient to predict thyroid cancer in endemic regions?
    Gamze ÇITLAK, Bahar CANBAY TORUN
    Journal of Surgery and Medicine.2020; 4(9): 794.     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
  • Nuclear features of papillary thyroid carcinoma: Comparison of Core needle biopsy and thyroidectomy specimens
    Jae Yeon Seok, Jungsuk An, Hyun Yee Cho, Younghye Kim, Seung Yeon Ha
    Annals of Diagnostic Pathology.2018; 32: 35.     CrossRef
  • Clinical utility of EZH1 mutations in the diagnosis of follicular-patterned thyroid tumors
    Chan Kwon Jung, Yourha Kim, Sora Jeon, Kwanhoon Jo, Sohee Lee, Ja Seong Bae
    Human Pathology.2018; 81: 9.     CrossRef
  • The History of Korean Thyroid Pathology
    Soon Won Hong, Chan Kwon Jung
    International Journal of Thyroidology.2018; 11(1): 15.     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
  • 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
    Journal of Pathology and Translational Medicine.2017; 51(6): 521.     CrossRef
  • Current Practices of Thyroid Fine-Needle Aspiration in Asia: A Missing Voice
    Andrey Bychkov, Kennichi Kakudo, SoonWon Hong
    Journal of Pathology and Translational Medicine.2017; 51(6): 517.     CrossRef
  • Current Status of Thyroid Fine-Needle Aspiration Practice in Thailand
    Somboon Keelawat, Samreung Rangdaeng, Supinda Koonmee, Tikamporn Jitpasutham, Andrey Bychkov
    Journal of Pathology and Translational Medicine.2017; 51(6): 565.     CrossRef
Case Reports
Spindle Cell Epithelioma, a So-called Benign Mixed Tumor of the Vagina: A Case Report.
Mee Hye Oh, Eun Ah Jung, Ji Hye Lee, Hyun Deuk Cho, Seung Ha Yang, Jeong Ja Kwak
Korean J Pathol. 2010;44(6):670-674.
DOI: https://doi.org/10.4132/KoreanJPathol.2010.44.6.670
  • 3,542 View
  • 61 Download
AbstractAbstract PDF
We report a case of spindle cell epithelioma, a so-called benign mixed tumor of the vagina. The patient was a 35-year-old nulliparous woman who presented with a polypoid mass in the posterior wall of the lower vagina just above the hymenal ring. The tumor was relatively well-defined with an expansile margin and composed of stromal-type spindle cells with a myxoid stroma arranged in short fascicles and an irregular cord-like or reticular pattern. A few glandular structures lined by cuboidal cells with squamous metaplasia were also noted. Cellular atypia was not conspicuous and mitosis was not found. We examined this tumor immunohistochemically to identify the histogenesis. The coexpression of epithelial and mesenchymal markers in stromal-type spindle cells suggested a multipotential cell origin for this tumor. The patient has been well with no signs of recurrence during the 12 months after surgery.
Pneumocystis carinii Pneumonia Presented as Diffuse Alveolar Damage: Report of a case.
Sook Kim, Jeong Ja Kwak, Dong Won Kim, So Young Jin, Dong Wha Lee
Korean J Pathol. 1996;30(12):1155-1158.
  • 1,865 View
  • 27 Download
AbstractAbstract PDF
Pneumocystis carinii is the most common cause of diffuse pulmonary infiltrates in the immunocompromised patients. Microscopically, Pneumocystis carinii pneumonia(PCP) shows characteristic frothy intraalveolar exudate and interstitial lymphocytic and plasma cell infiltrate. However, sometimes the only histologic finding of PCP on routine hematoxylin-eosin stain is that of diffuse alveolar damage(DAD), when we can miss the diagnosis without aid of special stains. We report a case of Pneumocystis carinii pneumonia presenting as DAD in a 50-year old man after chemotherapy due to malignant lymphoma. Open lung biopsy specimen reveals the early stage of DAD without any characteristic findings, such as foamy exudate. However many cysts of Pneumocystis carinii were found on Gomori's methenamine silver(GMS) stain. Therefore, GMS stain should be routinely performed on all biopsy specimens obtained from immunocompromised patients.
Original Articles
Fine needle aspiration cytology of apocrine carcinoma of the breast: two cases report-.
So Young Jin, Dong Wha Lee, Jeong Ja Kwak
Korean J Cytopathol. 1992;3(2):67-74.
  • 1,579 View
  • 12 Download
AbstractAbstract PDF
No abstract available.
Fine needle aspiration cytology of Ki-1 positive large cell lymphoma-a case report-.
Kye Hyun Kwon, Jeong Ja Kwak, So Young Jin, Dong Wha Lee
Korean J Cytopathol. 1993;4(2):127-132.
  • 1,434 View
  • 11 Download
AbstractAbstract PDF
No abstract available.
Fine needle aspiration cytology of langerhans cell histiocytosis.
Jeong Ja Kwak, So Young Jin, Dong Wha Lee
Korean J Cytopathol. 1993;4(2):140-145.
  • 1,656 View
  • 15 Download
AbstractAbstract PDF
No abstract available.
Ovarian Mucinous Adenocarcinoma Associated with Mucinous Adenocarcinoma of the Uterine Cervix.
Kye Hyun Kwon, Jeong Ja Kwak, So Young Jin, Dong Wha Lee
Korean J Pathol. 1995;29(2):244-247.
  • 2,355 View
  • 43 Download
AbstractAbstract PDF
When coexistence of carcinoma with similar histologic type is present in female genital tract, it is difficult to differentiate independent primary tumor from metastasis. Most of them are endometrial and ovarian tumors, but coexistence of uterine cervical and ovarian tumor with similar histologic type is rare. We experienced an independent primary tumor of ovarian mucinous cystadenocarcinoma associated with mucinous adenocarcinoma of uterine cervix. The patient was a 50-year-old woman. She had a lower abdominal mass which was detected as a huge cyst on ultrasonography. Although the ovarian lesions were bilateral, features that preferred to consider independent primary tumor are listed as; absence of lymphatic or vascular invasion, absence of ovarian surface implant, superficial invasion of cervical tumor, absence of tumor in abdominal cavity, and disease free follow-up after removal of the tumor.
Case Reports
Localized Pseudopolyposis of the Ascending Colon Associated with Granulomatous Colitis: A case report.
Jeong Ja Kwak, Kye Hyun Kwon, So Young Jin, Dong Wha Lee
Korean J Pathol. 1994;28(1):82-85.
  • 1,585 View
  • 15 Download
AbstractAbstract PDF
Pseudopolyps represent discrete areas of mucosal inflammation and regeneration that are seen in a variety of inflammatory bowel disease including ulcerative colitis and Crohn's disease. These polyps are typically short, measuring less than 1.5 cm in height. Rarely, localized giant pseudopolyposis can occur, i.e., a collection of larger inflammatory pseudopolyps giving rise to a mass lesion within the colon. The most serious problem concerned with pseudopolyposis is a confusion with carcinoma. We experienced a case of localized giant pseudopolyposis causing partial large bowel obstruction. Right hemicolectomy was done for a preoperative diagnosis of ascending colon carcinoma. The resected specimen contained a circumferential lesion, which was composed of numerous interconnecting cylindrical villi, measuring 12 cm in length and 3 cm in height. Microscopically, these polypoid lesions were inflammatory pseudopolyps. Several deep fissure-like ulcerations were noted with multifocal microabscess, lymphoid hyperplasia and an area of noncaseating granuloma.
Peutz-Jeghers Syndrome with Extensive Epithelial Misplacements and Adenomatous and Carcinomatous Transformation: A case report.
Jeong Ja Kwak, So Young Jin, Dong Wha Lee
Korean J Pathol. 1993;27(6):630-637.
  • 1,619 View
  • 17 Download
AbstractAbstract PDF
Peutz-Jeghers syndrome is an autosomal dominant disease characterized by gastrointestinal ployposis and mucocutaneous melanin pigmentation involving the lip, oral mucosa, digits, palms and soles. The polyps are almost hamartomatous. The relationship of gastrointestinal carcinoma and the Peutz-Jeghers syndrome has been discussed for many years. The question is unsettled whether gastrointestinal carcinoma arise in hamartomatous polyps itself. Recently, there are a few reports that adenomatous and carcinomatous changes were superimposed upon the background of the hamartoma. Occasionally epithelial misplacement of the epithelium is found in the small intestinal polyps. Since the epithelial misplacement may involve submucosa, muscularis propria and serosa, a difficulty of histopathologic differential diagnosis between the epithelial misplacement and invasive adenocarcinoma cause overdiagnosis of cancer in the gastrointestinal polyps of Peutz-Jeghers syndrome. We present a case of Peutz-Jeghers syndrome of 39-year-old woman with multiple gastrointestinal polyps, two of which showed extensive epithelial misplacement even into the pancreas and another one at the colon showed carcinomatous change at the tip portion. Areas of hamartoma, adenoma and in situ carcinoma were noted in this colonic hamartomatous polyp. This case support that adenoma and carcinomatous changes may evolve directly within a hamartomaous polyp itself.

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