Journal of Pathology and Translational Medicine

Letter To The Editor

Response to comment on “A stepwise approach to fine needle aspiration cytology of lymph nodes”: Yosep Chong, Gyeongsin Park, Hee Jeong Cha, Hyun-Jung Kim, Chang Suk Kang, Jamshid Abdul-Ghafar, Seung-Sook Lee; J Pathol Transl Med. 2024;58(1):43-44. Published online January 10, 2024; DOI: https://doi.org/10.4132/jptm.2023.12.04

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Original Article

Diagnostic proficiency test using digital cytopathology and comparative assessment of whole slide images of cytologic samples for quality assurance program in Korea: Yosep Chong, Soon Auck Hong, Hoon Kyu Oh, Soo Jin Jung, Bo-Sung Kim, Ji Yun Jeong, Ho-Chang Lee, Gyungyub Gong; J Pathol Transl Med. 2023;57(5):251-264. Published online August 24, 2023; DOI: https://doi.org/10.4132/jptm.2023.07.17

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Abstract PDF Supplementary Material: Background
The Korean Society for Cytopathology introduced a digital proficiency test (PT) in 2021. However, many doubtful opinions remain on whether digitally scanned images can satisfactorily present subtle differences in the nuclear features and chromatin patterns of cytological samples.
Methods
We prepared 30 whole-slide images (WSIs) from the conventional PT archive by a selection process for digital PT. Digital and conventional PT were performed in parallel for volunteer institutes, and the results were compared using feedback. To assess the quality of cytological assessment WSIs, 12 slides were collected and scanned using five different scanners, with four cytopathologists evaluating image quality through a questionnaire.
Results
Among the 215 institutes, 108 and 107 participated in glass and digital PT, respectively. No significant difference was noted in category C (major discordance), although the number of discordant cases was slightly higher in the digital PT group. Leica, 3DHistech Pannoramic 250 Flash, and Hamamatsu NanoZoomer 360 systems showed comparable results in terms of image quality, feature presentation, and error rates for most cytological samples. Overall satisfaction was observed with the general convenience and image quality of digital PT.
Conclusions
As three-dimensional clusters are common and nuclear/chromatin features are critical for cytological interpretation, careful selection of scanners and optimal conditions are mandatory for the successful establishment of digital quality assurance programs in cytology.

Review

A stepwise approach to fine needle aspiration cytology of lymph nodes: Yosep Chong, Gyeongsin Park, Hee Jeong Cha, Hyun-Jung Kim, Chang Suk Kang, Jamshid Abdul-Ghafar, Seung-Sook Lee; J Pathol Transl Med. 2023;57(4):196-207. Published online July 11, 2023; DOI: https://doi.org/10.4132/jptm.2023.06.12

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Abstract PDF Supplementary Material

The cytological diagnosis of lymph node lesions is extremely challenging because of the diverse diseases that cause lymph node enlargement, including both benign and malignant or metastatic lymphoid lesions. Furthermore, the cytological findings of different lesions often resemble one another. A stepwise diagnostic approach is essential for a comprehensive diagnosis that combines: clinical findings, including age, sex, site, multiplicity, and ultrasonography findings; low-power reactive, metastatic, and lymphoma patterns; high-power population patterns, including two populations of continuous range, small monotonous pattern and large monotonous pattern; and disease-specific diagnostic clues including granulomas and lymphoglandular granules. It is also important to remember the histological features of each diagnostic category that are common in lymph node cytology and to compare them with cytological findings. It is also essential to identify a few categories of diagnostic pitfalls that often resemble lymphomas and easily lead to misdiagnosis, particularly in malignant small round cell tumors, poorly differentiated squamous cell carcinomas, and nasopharyngeal undifferentiated carcinoma. Herein, we review a stepwise approach for fine needle aspiration cytology of lymphoid diseases and suggest a diagnostic algorithm that uses this approach and the Sydney classification system.

Citations

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Immunocytochemical markers, molecular testing and digital cytopathology for aspiration cytology of metastatic breast carcinoma
Joshua J. X. Li, Gary M. Tse
Cytopathology.2024; 35(2): 218. CrossRef
Response to comment on “A stepwise approach to fine needle aspiration cytology of lymph nodes”
Yosep Chong, Gyeongsin Park, Hee Jeong Cha, Hyun-Jung Kim, Chang Suk Kang, Jamshid Abdul-Ghafar, Seung-Sook Lee
Journal of Pathology and Translational Medicine.2024; 58(1): 43. CrossRef
Comment on “A stepwise approach to fine needle aspiration cytology of lymph nodes”
Elisabetta Maffei, Valeria Ciliberti, Pio Zeppa, Alessandro Caputo
Journal of Pathology and Translational Medicine.2024; 58(1): 40. CrossRef

Original Articles

Development of quality assurance program for digital pathology by the Korean Society of Pathologists: Yosep Chong, Jeong Mo Bae, Dong Wook Kang, Gwangil Kim, Hye Seung Han; J Pathol Transl Med. 2022;56(6):370-382. Published online November 15, 2022; DOI: https://doi.org/10.4132/jptm.2022.09.30

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Abstract PDF Supplementary Material

Background
Digital pathology (DP) using whole slide imaging is a recently emerging game changer technology that can fundamentally change the way of working in pathology. The Digital Pathology Study Group (DPSG) of the Korean Society of Pathologists (KSP) published a consensus report on the recommendations for pathologic practice using DP. Accordingly, the need for the development and implementation of a quality assurance program (QAP) for DP has been raised.
Methods
To provide a standard baseline reference for internal and external QAP for DP, the members of the Committee of Quality Assurance of the KSP developed a checklist for the Redbook and a QAP trial for DP based on the prior DPSG consensus report. Four leading institutes participated in the QAP trial in the first year, and we gathered feedback from these institutes afterwards.
Results
The newly developed checklists of QAP for DP contain 39 items (216 score): eight items for quality control of DP systems; three for DP personnel; nine for hardware and software requirements for DP systems; 15 for validation, operation, and management of DP systems; and four for data security and personal information protection. Most participants in the QAP trial replied that continuous education on unfamiliar terminology and more practical experience is demanding.
Conclusions
The QAP for DP is essential for the safe implementation of DP in pathologic practice. Each laboratory should prepare an institutional QAP according to this checklist, and consecutive revision of the checklist with feedback from the QAP trial for DP needs to follow.

Citations

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Diagnostic proficiency test using digital cytopathology and comparative assessment of whole slide images of cytologic samples for quality assurance program in Korea
Yosep Chong, Soon Auck Hong, Hoon Kyu Oh, Soo Jin Jung, Bo-Sung Kim, Ji Yun Jeong, Ho-Chang Lee, Gyungyub Gong
Journal of Pathology and Translational Medicine.2023; 57(5): 251. CrossRef

Current status of cytopathology practice in Korea: impact of the coronavirus pandemic on cytopathology practice: Soon Auck Hong, Haeyoen Jung, Sung Sun Kim, Min-Sun Jin, Jung-Soo Pyo, Ji Yun Jeong, Younghee Choi, Gyungyub Gong, Yosep Chong; J Pathol Transl Med. 2022;56(6):361-369. Published online October 27, 2022; DOI: https://doi.org/10.4132/jptm.2022.09.21

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Abstract PDF Supplementary Material

Background
The Continuous Quality Improvement program for cytopathology in 2020 was completed during the coronavirus pandemic. In this study, we report the result of the quality improvement program.
Methods
Data related to cytopathology practice from each institute were collected and processed at the web-based portal. The proficiency test was conducted using glass slides and whole-slide images (WSIs). Evaluation of the adequacy of gynecology (GYN) slides from each institution and submission of case glass slides and WSIs for the next quality improvement program were performed.
Results
A total of 214 institutions participated in the annual cytopathology survey in 2020. The number of entire cytopathology specimens was 8,220,650, a reduction of 19.0% from the 10,111,755 specimens evaluated in 2019. Notably, the number of respiratory cytopathology specimens, including sputum and bronchial washing/ brushing significantly decreased by 86.9% from 2019, which could be attributed to the global pandemic of coronavirus disease. The ratio of cases with atypical squamous cells to squamous intraepithelial lesions was 4.10. All participating institutions passed the proficiency test and the evaluation of adequacy of GYN slides.
Conclusions
Through the Continuous Quality Improvement program, the effect of coronavirus disease 2019 pandemic, manifesting with a reduction in the number of cytologic examinations, especially in respiratory-related specimen has been identified. The Continuous Quality Improvement Program of the Korean Society for Cytopathology can serve as the gold standard to evaluate the current status of cytopathology practice in Korea.

Citations

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A stepwise approach to fine needle aspiration cytology of lymph nodes
Yosep Chong, Gyeongsin Park, Hee Jeong Cha, Hyun-Jung Kim, Chang Suk Kang, Jamshid Abdul-Ghafar, Seung-Sook Lee
Journal of Pathology and Translational Medicine.2023; 57(4): 196. CrossRef
Diagnostic proficiency test using digital cytopathology and comparative assessment of whole slide images of cytologic samples for quality assurance program in Korea
Yosep Chong, Soon Auck Hong, Hoon Kyu Oh, Soo Jin Jung, Bo-Sung Kim, Ji Yun Jeong, Ho-Chang Lee, Gyungyub Gong
Journal of Pathology and Translational Medicine.2023; 57(5): 251. CrossRef

Review

Recommendations for pathologic practice using digital pathology: consensus report of the Korean Society of Pathologists: Yosep Chong, Dae Cheol Kim, Chan Kwon Jung, Dong-chul Kim, Sang Yong Song, Hee Jae Joo, Sang-Yeop Yi; J Pathol Transl Med. 2020;54(6):437-452. Published online October 8, 2020; DOI: https://doi.org/10.4132/jptm.2020.08.27

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Abstract PDF Supplementary Material

Digital pathology (DP) using whole slide imaging (WSI) is becoming a fundamental issue in pathology with recent advances and the rapid development of associated technologies. However, the available evidence on its diagnostic uses and practical advice for pathologists on implementing DP remains insufficient, particularly in light of the exponential growth of this industry. To inform DP implementation in Korea, we developed relevant and timely recommendations. We first performed a literature review of DP guidelines, recommendations, and position papers from major countries, as well as a review of relevant studies validating WSI. Based on that information, we prepared a draft. After several revisions, we released this draft to the public and the members of the Korean Society of Pathologists through our homepage and held an open forum for interested parties. Through that process, this final manuscript has been prepared. This recommendation contains an overview describing the background, objectives, scope of application, and basic terminology; guidelines and considerations for the hardware and software used in DP systems and the validation required for DP implementation; conclusions; and references and appendices, including literature on DP from major countries and WSI validation studies.

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Diagnostic proficiency test using digital cytopathology and comparative assessment of whole slide images of cytologic samples for quality assurance program in Korea
Yosep Chong, Soon Auck Hong, Hoon Kyu Oh, Soo Jin Jung, Bo-Sung Kim, Ji Yun Jeong, Ho-Chang Lee, Gyungyub Gong
Journal of Pathology and Translational Medicine.2023; 57(5): 251. CrossRef
Real-World Implementation of Digital Pathology: Results From an Intercontinental Survey
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Development of quality assurance program for digital pathology by the Korean Society of Pathologists
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Original Articles

A machine-learning expert-supporting system for diagnosis prediction of lymphoid neoplasms using a probabilistic decision-tree algorithm and immunohistochemistry profile database: Yosep Chong, Ji Young Lee, Yejin Kim, Jingyun Choi, Hwanjo Yu, Gyeongsin Park, Mee Yon Cho, Nishant Thakur; J Pathol Transl Med. 2020;54(6):462-470. Published online August 31, 2020; DOI: https://doi.org/10.4132/jptm.2020.07.11

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Abstract PDF Supplementary Material

Background
Immunohistochemistry (IHC) has played an essential role in the diagnosis of hematolymphoid neoplasms. However, IHC interpretations can be challenging in daily practice, and exponentially expanding volumes of IHC data are making the task increasingly difficult. We therefore developed a machine-learning expert-supporting system for diagnosing lymphoid neoplasms.
Methods
A probabilistic decision-tree algorithm based on the Bayesian theorem was used to develop mobile application software for iOS and Android platforms. We tested the software with real data from 602 training and 392 validation cases of lymphoid neoplasms and compared the precision hit rates between the training and validation datasets.
Results
IHC expression data for 150 lymphoid neoplasms and 584 antibodies was gathered. The precision hit rates of 94.7% in the training data and 95.7% in the validation data for lymphomas were not statistically significant. Results in most B-cell lymphomas were excellent, and generally equivalent performance was seen in T-cell lymphomas. The primary reasons for lack of precision were atypical IHC profiles for certain cases (e.g., CD15-negative Hodgkin lymphoma), a lack of disease-specific markers, and overlapping IHC profiles of similar diseases.
Conclusions
Application of the machine-learning algorithm to diagnosis precision produced acceptable hit rates in training and validation datasets. Because of the lack of origin- or disease- specific markers in differential diagnosis, contextual information such as clinical and histological features should be taken into account to make proper use of this system in the pathologic decision-making process.

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Validation of a Machine Learning Expert Supporting System, ImmunoGenius, Using Immunohistochemistry Results of 3000 Patients with Lymphoid Neoplasms
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Current status of cytopathology practices in Korea: annual report on the Continuous Quality Improvement program of the Korean Society for Cytopathology for 2018: Yosep Chong, Haeyoen Jung, Jung-Soo Pyo, Soon Won Hong, Hoon Kyu Oh; J Pathol Transl Med. 2020;54(4):318-331. Published online April 15, 2020; DOI: https://doi.org/10.4132/jptm.2020.02.26

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Abstract PDF Supplementary Material

Background
The Korean Society for Cytopathology has conducted the Continuous Quality Improvement program for cytopathology laboratories in Korea since 1995. In 2018 as part of the program, an annual survey of cytologic data was administered to determine the current status of cytopathology practices in Korea. Methods: A questionnaire was administered to 211 cytopathology laboratories. Individual laboratories submitted their annual statistics regarding cytopathology practices, diagnoses of gynecologic samples, inadequacy rates, and gynecologic cytology-histology correlation review (CHCR) data for 2018. In addition, proficiency tests and sample adequacy assessments were conducted using five consequent gynecologic slides. Results: Over 10 million cytologic exams were performed in 2018, and this number has almost tripled since this survey was first conducted in 2004 (compounded annual growth rate of 7.2%). The number of non-gynecologic samples has increased gradually over time and comprised 24% of all exams. The overall unsatisfactory rate was 0.14%. The ratio of the cases with atypical squamous cells to squamous intraepithelial lesions accounted for up to 4.24. The major discrepancy rate of the CHCR in gynecologic samples was 0.52%. In the proficiency test, the major discrepancy rate was approximately 1%. In the sample adequacy assessment, a discrepancy was observed in 0.1% of cases. Conclusions: This study represents the current status of cytopathology practices in Korea, illustrating the importance of the Continuous Quality Improvement program for increasing the accuracy and credibility of cytopathologic exams as well as developing national cancer exam guidelines and government projects on the prevention and treatment of cancer.

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Diagnostic proficiency test using digital cytopathology and comparative assessment of whole slide images of cytologic samples for quality assurance program in Korea
Yosep Chong, Soon Auck Hong, Hoon Kyu Oh, Soo Jin Jung, Bo-Sung Kim, Ji Yun Jeong, Ho-Chang Lee, Gyungyub Gong
Journal of Pathology and Translational Medicine.2023; 57(5): 251. CrossRef
Recent Application of Artificial Intelligence in Non-Gynecological Cancer Cytopathology: A Systematic Review
Nishant Thakur, Mohammad Rizwan Alam, Jamshid Abdul-Ghafar, Yosep Chong
Cancers.2022; 14(14): 3529. CrossRef
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Chan Kwon Jung, Ja Seong Bae, Young Joo Park
Endocrinology and Metabolism.2022; 37(5): 816. CrossRef
Current status of cytopathology practice in Korea: impact of the coronavirus pandemic on cytopathology practice
Soon Auck Hong, Haeyoen Jung, Sung Sun Kim, Min-Sun Jin, Jung-Soo Pyo, Ji Yun Jeong, Younghee Choi, Gyungyub Gong, Yosep Chong
Journal of Pathology and Translational Medicine.2022; 56(6): 361. CrossRef

Review

Introduction to digital pathology and computer-aided pathology: Soojeong Nam, Yosep Chong, Chan Kwon Jung, Tae-Yeong Kwak, Ji Youl Lee, Jihwan Park, Mi Jung Rho, Heounjeong Go; J Pathol Transl Med. 2020;54(2):125-134. Published online February 13, 2020; DOI: https://doi.org/10.4132/jptm.2019.12.31

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Abstract PDF

Digital pathology (DP) is no longer an unfamiliar term for pathologists, but it is still difficult for many pathologists to understand the engineering and mathematics concepts involved in DP. Computer-aided pathology (CAP) aids pathologists in diagnosis. However, some consider CAP a threat to the existence of pathologists and are skeptical of its clinical utility. Implementation of DP is very burdensome for pathologists because technical factors, impact on workflow, and information technology infrastructure must be considered. In this paper, various terms related to DP and computer-aided pathologic diagnosis are defined, current applications of DP are discussed, and various issues related to implementation of DP are outlined. The development of computer-aided pathologic diagnostic tools and their limitations are also discussed.

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Brief Case Reports

Mucosal Schwann Cell Hamartoma in Colorectal Mucosa: A Rare Benign Lesion That Resembles Gastrointestinal Neuroma: Jiheun Han, Yosep Chong, Tae-Jung Kim, Eun Jung Lee, Chang Suk Kang; J Pathol Transl Med. 2017;51(2):187-189. Published online August 25, 2016; DOI: https://doi.org/10.4132/jptm.2016.07.02

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Multiple non-polypoid mucosal Schwann cell hamartomas presenting as edematous and submucosal tumor-like lesions: a case report
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Necrotizing Sarcoid Granulomatosis: Possibly Veiled Disease in Endemic Area of Mycobacterial Infection: Yosep Chong, Eun Jung Lee, Chang Suk Kang, Tae-Jung Kim, Jung Sup Song, Hyosup Shim; J Pathol Transl Med. 2015;49(4):346-350. Published online June 1, 2015; DOI: https://doi.org/10.4132/jptm.2015.04.17

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Original Article

Histologic Disorderliness in the Arrangement of Tumor Cells as an Objective Measure of Tumor Differentiation: Sungwook Suh, Gyeongsin Park, Young Sub Lee, Yosep Chong, Youn Soo Lee, Yeong Jin Choi; Korean J Pathol. 2014;48(5):339-345. Published online October 27, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.5.339

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Abstract PDF: Background: Inter-observer and intra-observer variation in histologic tumor grading are well documented. To determine whether histologic disorderliness in the arrangement of tumor cells may serve as an objective criterion for grading, we tested the hypothesis the degree of disorderliness is related to the degree of tumor differentiation on which tumor grading is primarily based. Methods: Borrowing from the statistical thermodynamic definition of entropy, we defined a novel mathematical formula to compute the relative degree of histologic disorderliness of tumor cells. We then analyzed a total of 51 photomicrographs of normal colorectal mucosa and colorectal adenocarcinoma with varying degrees of differentiation using our formula. Results: A one-way analysis of variance followed by post hoc pairwise comparisons using Bonferroni correction indicated that the mean disorderliness score was the lowest for the normal colorectal mucosa and increased with decreasing tumor differentiation. Conclusions: Disorderliness, a pathologic feature of malignant tumors that originate from highly organized structures is useful as an objective tumor grading proxy in the field of digital pathology.

Brief Case Report

Fine Needle Aspiration Cytology of Warthin-like Papillary Thyroid Carcinoma: A Brief Case Report: Yosep Chong, Sungwook Suh, Tae-Jung Kim, Eun Jung Lee; Korean J Pathol. 2014;48(2):170-173. Published online April 28, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.2.170

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Citations

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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
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
Solid papillary thyroid carcinoma with Hashimoto’s thyroiditis: description of a further case with challenging cytological features
Franco Fulciniti, Jessica Barizzi, Pierpaolo Trimboli, Luca Giovanella
BMJ Case Reports.2019; 12(1): e226153. CrossRef
Preoperative Cytologic Diagnosis of Warthin-like Variant of Papillary Thyroid Carcinoma
Jisup Kim, Beom Jin Lim, Soon Won Hong, Ju Yeon Pyo
Journal of Pathology and Translational Medicine.2018; 52(2): 105. CrossRef
Warthin like papillary carcinoma - A rare variant of papillary carcinoma thyroid
Mir Wajahat, Tazeen Jeelani, Kanika Gupta, Nusrat Bashir
Human Pathology: Case Reports.2018; 13: 21. CrossRef
Cytological features of warthin‐like papillary thyroid carcinoma: A case report with review of previous cytology cases
Archana George Vallonthaiel, Shipra Agarwal, Deepali Jain, Rajni Yadav, Nishikant A. Damle
Diagnostic Cytopathology.2017; 45(9): 837. CrossRef
Comparison of EASYPREP® and SurePath® in thyroid fine‐needle aspiration
Yosep Chong, Ki Hyun Baek, Jee Young Kim, Tae‐Jung Kim, Eun Jung Lee, Chang Suk Kang
Diagnostic Cytopathology.2016; 44(4): 283. CrossRef
Ultrasonographic features and clinical characteristics of Warthin-like variant of papillary thyroid carcinoma
Ga Ram Kim, Jung Hee Shin, Soo Yeon Hahn, Eun Young Ko, Young Lyun Oh
Endocrine Journal.2016; 63(4): 329. CrossRef
Warthin-Like Papillary Thyroid Carcinoma Associated with Lymphadenopathy and Hashimoto’s Thyroiditis
Karla Judith González-Colunga, Abelardo Loya-Solis, Luis Ángel Ceceñas-Falcón, Oralia Barboza-Quintana, René Rodríguez-Gutiérrez
Case Reports in Endocrinology.2015; 2015: 1. CrossRef
Tumeur Warthin-like de la thyroïde : à propos d’un cas
W. Rekik, A. Khadhar, A. Zehani, H. Azouz, I. Chelly, T. Ben Ghachem, A. Sellem, M. Tounsi, H. Ben Mahjouba, S. Haouet, N. Kchir
Journal Africain du Cancer / African Journal of Cancer.2015; 7(4): 247. CrossRef

Case Report

First Report of a Gangliocytic Paraganglioma Arising in a Tailgut Cyst.: Yosep Chong, Mee Yon Cho; Korean J Pathol. 2010;44(4):435-440.; DOI: https://doi.org/10.4132/KoreanJPathol.2010.44.4.435

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Abstract PDF

Here we present the first report of a gangliocytic paraganglioma arising in a tailgut cyst; it occurred in a 56-year-old man. Tailgut cysts are uncommon congenital hamartomatous lesions that arise in the retrorectal presacral space in infants or adults. Benign or malignant tumors associated with tailgut cysts are rarely described; the most common tumors are adenocarcinomas and carcinoid tumors. A gangliocytic paraganglioma is a rare benign tumor that occurs nearly exclusively in the second portion of the duodenum. Rare cases have been reported at other locations, but a tailgut cyst has never been described. In our case, a resected 3.9 x 3.3 x 3 cm mass was composed predominantly of a solid yellow white neuroendocrine tumor within the area of a tailgut cyst. The neuroendocrine component of this tumor was different from previously described carcinoid tumors with respect to the histologic findings of neural differentiation as well as the intermixed typical gangliocytic features highlighted by immunohistochemical stains for S-100 protein and neurofilament. Although an intermixed area of the tailgut cyst and gangliocytic paraganglioma were found in some areas, the pathogenesis of this tumor remains to be elucidated.

Citations

Citations to this article as recorded by

Diagnosis of Tailgut Cyst in Gynecologic Patients: Systematic Review of the Literature
Polina Schwarzman, Salvatore Andrea Mastrolia, Yael Sciaky-Tamir, Joel Baron, Boaz Sheizaf, Giuseppe Trojano, Reli Hershkovitz
Journal of Endometriosis and Pelvic Pain Disorders.2017; 9(3): 168. CrossRef
Fine Needle Aspiration Cytology Diagnosis of Tailgut Cyst: A Rare Entity
Farhan Asif Siddiqui, Rajan Chopra, Yusef Al-Marzooq
Acta Cytologica.2014; 58(2): 217. CrossRef

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