Journal of Pathology and Translational Medicine

Volume 54(6); November 2020

Reviews

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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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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Liquid biopsy using extracellular vesicle–derived DNA in lung adenocarcinoma: In Ae Kim, Jae Young Hur, Hee Joung Kim, Seung Eun Lee, Wan Seop Kim, Kye Young Lee; J Pathol Transl Med. 2020;54(6):453-461. Published online October 8, 2020; DOI: https://doi.org/10.4132/jptm.2020.08.13

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Abstract PDF

Blood liquid biopsy has emerged as a way of overcoming the clinical limitations of repeat biopsy by testing for the presence of acquired resistance mutations to therapeutic agents. Despite its merits of repeatability and non-invasiveness, this method is currently only used as a supplemental test due to a relatively low sensitivity rate of 50%–60%, and cannot replace tissue biopsy. The circulating tumor DNAs used in blood liquid biopsies are passive products of fragmented DNA with a short half-life released following tumor cell death; the low sensitivity seen with liquid blood biopsy results from this instability, which makes increasing the sensitivity of this test fundamentally difficult. Extracellular vesicles (EVs) are ideal carriers of cancer biomarkers, as cancer cells secret an abundance of EVs, and the contents of tumor cell-originated EVs reflect the molecular and genetic composition of parental cells. In addition, EV-derived DNAs (EV DNAs) consist of large-sized genomic DNAs and tumor-specific oncogenic mutant DNAs. For these reasons, liquid biopsy using EV DNA has the potential to overcome issues arising from tissue shortages associated with small biopsies, which are often seen in lung cancer patients, and the biopsy product can be used in other diagnostic methods, such as epidermal growth factor receptor (EGFR) mutation testing and next-generation sequencing (NGS). A higher sensitivity can be achieved when EV DNAs obtained from bronchoalveolar lavage fluid (BALF) are used rather than those from blood. BALF, when obtained close to the tumor site, is a promising liquid biopsy tool, as it enables the gathering of both cellular and non-cellular fractions of the tumor microenvironment, and provides increased diagnostic sensitivity when compared to blood.

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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
Jamshid Abdul-Ghafar, Kyung Jin Seo, Hye-Ra Jung, Gyeongsin Park, Seung-Sook Lee, Yosep Chong
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Muhammad Joan Ailia, Nishant Thakur, Jamshid Abdul-Ghafar, Chan Kwon Jung, Kwangil Yim, Yosep Chong
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Diagnosis prediction of tumours of unknown origin using ImmunoGenius, a machine learning-based expert system for immunohistochemistry profile interpretation
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The frequency of POLE-mutation in endometrial carcinoma and prognostic implications: a systemic review and meta-analysis: Alaa Salah Jumaah, Mais Muhammed Salim, Hawraa Sahib Al-Haddad, Katherine Ann McAllister, Akeel Abed Yasseen; J Pathol Transl Med. 2020;54(6):471-479. Published online September 2, 2020; DOI: https://doi.org/10.4132/jptm.2020.07.23

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Abstract PDF Supplementary Material

Background
Endometrial carcinoma (EC) is classified into four distinct molecular subgroups including ultramutated DNA polymerase epsilon (POLE). POLE-mutated tumors have the best prognosis and are a promising target for immunotherapy. This meta-analysis consolidated the reported variation of POLE-mutant frequency and assessed prognostic value in EC.
Methods
Internet searches explored scientific data bases: EMBASE, PubMed, and the Cochrane Central Register of Controlled Trials databases. Data was extracted from eligible studies including: sample size, number of positive POLE-mutant cases, sequencing information, clinicopathologic data, and survival data. Meta-analysis and a random-effects model produced pooled estimates of POLE frequency and prognostic parameters using 95% confidence intervals (CI), hazard ratios (HR), and odd ratios (OR).
Results
Six thousand three hundred and forty-six EC patient cases were pooled from 25 studies. The pooled proportion of POLE gene mutation in EC was 8.59% (95% CI, 7.01 to 10.32), of which 8.22% (95% CI, 6.27 to 10.42) were type I and 0.93% (95% CI, 0.34 to 1.81) type 2. Clinicopathologic data showed that POLE-mutated tumors are mostly endometrioid. They present at higher levels in earlier stages (I–II) of EC (89.51%; 95% CI, 81.11 to 95.66) at the highest grade III (51.53%; 95% CI, 36.08 to 66.84) with reduced myometrial invasion (OR, 1.48, 95% CI, 0.99 to 2.20). Survival analysis indicated favorable overall survival (HR, 0.90), disease-specific survival (HR, 0.41), and progression-free survival (HR, 0.23) for POLE mutant EC.
Conclusions
Almost one-tenth of EC patients have POLE-mutated tumors. Given their improved prognostic potential, identifying the POLE mutation status is key for the management of EC patients.

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Evaluation of human papillomavirus (HPV) prediction using the International Endocervical Adenocarcinoma Criteria and Classification system, compared to p16 immunohistochemistry and HPV RNA in-situ hybridization: Hezhen Ren, Jennifer Pors, Christine Chow, Monica Ta, Simona Stolnicu, Robert Soslow, David Huntsman, Lynn Hoang; J Pathol Transl Med. 2020;54(6):480-488. Published online August 31, 2020; DOI: https://doi.org/10.4132/jptm.2020.07.18

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Abstract PDF

Background
The International Endocervical Adenocarcinoma Criteria and Classification (IECC) separated endocervical adenocarcinomas into human papillomavirus (HPV) associated (HPVA) and non–HPV-associated (NHPVA) categories by morphology alone. Our primary objective was to assess the accuracy of HPV prediction by the IECC system compared to p16 immunohistochemistry and HPV RNA in-situ hybridization (RISH). Our secondary goal was to directly compare p16 and HPV RISH concordance.
Methods
Cases were classified by IECC and stained for p16 and HPV RISH on tissue microarray, with discordant p16/HPV RISH cases re-stained on whole tissue sections. Remaining discordant cases (p16/HPV, IECC/p16, IECC/HPV discordances) were re-reviewed by the original pathologists (n = 3) and external expert pathologists (n = 2) blinded to the p16 and HPV RISH results. Final IECC diagnosis was assigned upon independent agreement between all reviewers.
Results
One hundred and eleven endocervical adenocarcinomas were classified originally into 94 HPVA and 17 NHPVA cases. p16 and HPV RISH was concordant in 108/111 cases (97%) independent of the IECC. HPV RISH and p16 was concordant with IECC in 103/111 (93%) and 106/111 (95%), respectively. After expert review, concordance improved to 107/111 (96%) for HPV RISH. After review of the eight discordant cases, one remained as HPVA, four were reclassified to NHPVA from HPVA, two were unclassifiable, and one possibly represented a mixed usual and gastric-type adenocarcinoma.
Conclusions
p16 and HPV RISH have excellent concordance in endocervical adenocarcinomas, and IECC can predict HPV status in most cases. Focal apical mitoses and apoptotic debris on original review led to the misclassification of several NHPVA as HPVA.

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Linghui Lu, Tianqi Liu, Shunni Wang, Jing Li, Feiran Zhang, Yan Ning, Yiqin Wang
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Francesca Arezzo, Gennaro Cormio, Vera Loizzi, Gerardo Cazzato, Viviana Cataldo, Claudio Lombardi, Giuseppe Ingravallo, Leonardo Resta, Ettore Cicinelli
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Hezhen Ren, Noorah Almadani, Jennifer Pors, Samuel Leung, Julie Ho, Christine Chow, Monica Ta, Kay J. Park, Simona Stolnicu, Robert Soslow, David Huntsman, Blake C. Gilks, Lynn Hoang
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Primary squamous cell carcinoma of the salivary gland: immunohistochemical analysis and comparison with metastatic squamous cell carcinoma: Uiree Jo, Joon Seon Song, Seung-Ho Choi, Soon Yuhl Nam, Sang Yoon Kim, Kyung-Ja Cho; J Pathol Transl Med. 2020;54(6):489-496. Published online August 31, 2020; DOI: https://doi.org/10.4132/jptm.2020.07.19

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Background
Primary squamous cell carcinoma (SCC) of the salivary gland is a rare disease, and distinguishing primary SCC from metastatic SCC is difficult. This study investigated the histological and immunohistochemical differences between primary and metastatic salivary gland SCC to improve the accuracy of diagnosis and to explore the pathogenesis of this disease.
Methods
Data of 16 patients who underwent surgery for SCC of salivary glands between 2000 and 2018 at Asan Medical Center were retrieved. Eight patients had a history of SCC at other sites, and eight patients had only salivary gland SCC. Immunostaining for p16, p53, androgen receptor (AR), gross cystic disease fluid protein 15 (GCDFP-15), and c-erbB2, as well as mucicarmine staining, were compared between the two groups.
Results
Most tumors were located in the center of the salivary glands with extraparenchymal extension. The histology of primary SCC of the salivary gland was consistent with moderately differentiated SCC with extensive desmoplastic reaction and peritumoral inflammation. Involvement of the salivary gland ducts and transition into the ductal epithelium were observed in two cases. Metastatic SCC resembled the primary tumor histologically and was associated with central necrosis. Both groups exhibited negative mucin staining. Two, one, and one primary SCC case exhibited AR, GCDFP-15, and c-erbB2 positivity, respectively.
Conclusions
A subset of primary SCCs originated in salivary ducts or was related to salivary duct carcinoma. Distinguishing primary from metastatic SCC of the salivary gland is difficult using histologic features and immunoprofiles. A comprehensive review of the medical history is essential.

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A case of primary squamous cell carcinoma of the parotid gland and review of the literature
Jingli Zhao, Xinrong Nan, Chuhuan Zhou, Nan Jiang, Liangliang Tian
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Metastatic cutaneous squamous cell carcinoma accounts for nearly all squamous cell carcinomas of the parotid gland
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Can BAP1 expression loss in mesothelial cells be an indicator of malignancy?: Hanife Gulnihal Ozdemir, Sermin Coban Kokten, Nagehan Ozdemir Barisik; J Pathol Transl Med. 2020;54(6):497-503. Published online November 9, 2020; DOI: https://doi.org/10.4132/jptm.2020.09.14

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Background
Malignant mesothelioma is a highly aggressive tumor that can be confused with a benign mesothelial lesion, especially cytomorphologic lesions. BRCA1-associated protein 1 (BAP1) acts as a tumor suppressor. In this study, we aim to investigate the value of BAP1 staining of malignant mesothelioma cases with expression loss and diagnosis in cell block and biopsy tissue.
Methods
Between January 2009 and March 2017, 64 mesotheliomas, 117 reactive mesothelial hyperplasias, and 20 fibrinous pleuritis/pericarditis were diagnosed with morphologic and immunohistochemical findings in our pathology clinic and were included in the study. Formalin-fixed, paraffin-embedded tissues were immunohistochemically examined for BAP1. Inflammatory and stromal cells were used as positive internal controls. BAP1 was assessed for nuclear staining in mesothelial cells.
Results
Examinations of the relationship between patient diagnosis and BAP1 biopsy status showed that the BAP1 loss rate (76.6%) was significantly higher in malignant mesothelioma cases than in other benign diseases (0%) (p<.001). Sensitivity and specificity were 76.56% and 100%, respectively, for biopsy tissue from malignant mesothelioma. Sensitivity and specificity were both 100% for BAP1 test on cell block tissue. Furthermore, the consistency between BAP1 cell block and biopsy results was excellent (ĸ=0.90) and the correlation was significant (p<.001).
Conclusions
This study shows that BAP1 expression loss in both cytology and biopsy tissue in biopsy-confirmed malignant mesothelioma cases is an essential parameter for malignant mesothelioma diagnosis.

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Case Studies

A case of monoclonal gammopathy of renal significance presenting as atypical amyloidosis with IgA lambda paraproteinemia: Chankyung Kim, John Brealey, Anjelo Jobert, James Nolan; J Pathol Transl Med. 2020;54(6):504-507. Published online November 9, 2020; DOI: https://doi.org/10.4132/jptm.2020.09.18

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Abstract PDF

Monoclonal gammopathy of renal significance is defined as any B cell or plasma cell clonal lymphoproliferation which neither causes tumor complications nor meets any current hematological criteria for specific therapy, with one or more kidney lesions related to the produced monoclonal immunoglobulin, such as amyloidosis. A 50-year-old male presented with heavy proteinuria and blood tests showing IgA and Lambda paraproteinemia. Light microscopy showed mesangial eosinophilic ground substance extending into the capillary loops, and positive staining within the glomeruli and vessel walls for amyloid P immunohistochemistry was also noted. Immunofluorescence showed positive staining for IgA and Lambda in the mesangia and capillary loops. Electron microscopy exhibited organized fibrils measuring 4–5 nm in diameter in the mesangia, glomerular basement membranes and vessel walls. We interpreted the overall findings as atypical renal amyloidosis with IgA and Lambda deposition on immunofluorescence. Further amyloid typing using laser microdissection-liquid chromatography and mass spectrometry will be useful.

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Yuwei Zhou, Ziru Huang, Yushu Gou, Siqi Liu, Wei Yang, Hongyu Zhang, Anthony Mackitz Dzisoo, Jian Huang
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Intraoperative frozen cytology of intraosseous cystic meningioma in the sphenoid bone: Na Rae Kim, Gie-Taek Yie; J Pathol Transl Med. 2020;54(6):508-512. Published online July 1, 2020; DOI: https://doi.org/10.4132/jptm.2020.05.21

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Abstract PDF

Meningiomas in bone are rarely subjected to fine-needle aspiration diagnosis, and those arising in the skull bone with a cystic presentation are rare. A 24-year-old woman presented with subdural hemorrhage, and subsequent radiology depicted an osteolytic mass-like lesion in the sphenoid bone. Intraoperatively, a solid and cystic hemorrhagic lesion mimicking an aneurysmal bone cyst was observed in the sphenoid bone with dural tearing. Frozen cytology showed singly scattered or epithelioid clusters of round to elongated cells intermixed with many neutrophils. Tumor cells had bland-looking round nuclei with rare prominent nucleoli and nuclear inclusions and eosinophilic granular to globoid cytoplasm in capillary-rich fragments. Histology revealed intraosseous meningothelial and microcystic meningioma (World Health Organization grade 1) in right lesser wing of the sphenoid bone. Considering its unusual location and cytologic findings, differential diagnoses included chordoma, chondroma, chondrosarcoma, and aneurysmal bone cyst. The present case posed a diagnostic challenge due to possible confusion with these entities.

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Brief Case Report

Xanthogranulomatous endometritis: a report of two Korean cases with cytologic findings: Ji Min Na, Min Hye Kim, Gyung Hyuck Ko, Jeong Kyu Shin; J Pathol Transl Med. 2020;54(6):513-516. Published online October 23, 2020; DOI: https://doi.org/10.4132/jptm.2020.08.18

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PDF

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