Journal of Pathology and Translational Medicine

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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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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Original Articles

Extrapulmonary Lymphangioleiomyoma: Clinicopathological Analysis of 4 Cases: Dae Hyun Song, In Ho Choi, Sang Yun Ha, Kang Min Han, Jae Jun Lee, Min Eui Hong, Yoon-La Choi, Kee-Taek Jang, Sang Yong Song, Chin A Yi, Joungho Han; Korean J Pathol. 2014;48(3):188-192. Published online June 26, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.3.188

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Abstract PDF

Background

Lymphangioleiomyomatosis (LAM) is a slowly progressive neoplastic disease that predominantly affects females. Usually, LAM affects the lung; it can also affect extrapulmonary sites, such as the mediastinum, the retroperitoneum, or the lymph nodes, although these locations are rare. A localized form of LAM can manifest as extrapulmonary lesions; this form is referred to as extrapulmonary lymphangioleiomyoma (E-LAM). Due to the rare occurrence of E-LAM and its variable, atypical location, E-LAM is often difficult to diagnose. Herein, we report the clinicopathological information from four E-LAM cases, and also review previous articles investigating this disease.

Methods

Four patients with E-LAM were identified at the Samsung Medical Center (Seoul, Korea) from 1995 to 2012. All E-LAM lesions underwent surgical excision.

Results

All patients were females within the age range of 43 to 47 years. Two patients had para-aortic retroperitoneal masses, while the other two patients had pelvic lesions; two out of the four patients also had accompanying pulmonary LAM. In addition, no patient displayed any evidence of tuberous sclerosis. Histologically, two patients exhibited nuclear atypism with cytologic degeneration.

Conclusions

E-LAM should be considered in the differential diagnosis of patients presenting with pelvic or para-aortic masses. We also conclude that further clinical and pathological evaluation is needed in patients with E-LAM and nuclear atypism.

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Takashi Ogura, Nagio Takigawa, Keisuke Tomii, Kazuma Kishi, Yoshikazu Inoue, Eiki Ichihara, Sakae Homma, Kazuhisa Takahashi, Hiroaki Akamatsu, Satoshi Ikeda, Naohiko Inase, Tae Iwasawa, Yuichiro Ohe, Hiromitsu Ohta, Hiroshi Onishi, Isamu Okamoto, Kazumasa
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Expression of nm23 Protein in Breast Carcinoma: An immunohistochemical study.: Sang Yong Song, Je G Chi, Se Hwan Han, Kuk Jin Choe; Korean J Pathol. 1995;29(4):469-477.

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Abstract PDF: To elucidate a possible prognostic factor, we studied 91 cases of breast carcinoma for the expression of n-tn23 protein using an immunohistochemical method, and compared these results with the known prognostic parameters of the breast carcinoma. The mn23 protein was intensely stained in the cytoplasm and/or the nucleus of carcinoma cells in 82 cases(90.1%). There were two patterns of cytoplasmic staining; heterogeneous pattern and homogeneous pattern. Among the positive cases, 43 cases(47.2%) were heterogeneous while 39 cases(42.8%) were homogeneous. Axillary lymph node metastases(p<0.005) was found more frequently in the heterogeneous pattern group(79.0%) than in the homogeneous pattern group(41.0%). There was no significant correlation between nm23 protein expression and other parameters such as patient age, tumor size, estrogen receptor, histopathologic grade, and p53 overexpression. Although axillary lymph node metastasis was correlated with the disease free status(p<0.0005) and patient survival (p<0.05), they showed no correlation with nin23 expression. Multivariate analysis showed that axillary lymph node metastasis was the only prognostic indicator(p<0.05), and the expression of nm23 protein was of borderline significance. The results suggest that the homogeneous and/or granular cytoplasmic expression of mn23 protein plays a role in the suppression of nodal metastasis in breast carcinoma and might contribute in predicting patient survival.

Carcinoid Tumors of the Gastrointestinal Tract: Analysis of 36 Cases.: Kyeong Cheon Jung, Hee Sung Kim, Sang Yong Song, Ghee Young Choe, Yong Il Kim; Korean J Pathol. 1996;30(5):396-407.

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Abstract PDF: We reviewed a total of 36 cases of gastrointestinal carcinoid tumors during a period of ten and a half years at Seoul National University Hospital, looking at their histologic and ultrastructural features, as well as immunohistochemical results, then we correlated these with location. The primary sites of carcinoid tumors were rectum(39%), stomach(25%), appendix(22%), small intestine(8%) and colon(6%), in order of frequency. The predominant histologic types by organ were mixed and solid(A) types in all location, the solid type(type A) in the stomach, and tubular type(type C) in the rectum. Six out of 8 cases of appendiceal carcinoid were type A and the other two cases were mucinous carcinoid. Tubular adenoma or adenocarcinoma was associated with 36% of the rectal carcinoids, with one case of carcinoid in the small intestine, and one(11%) of the gastric carcinoids was found near an adenocarcinoma. Metastasis was found in one case of ileal carcinoid(100%), one case of cecal carcinoid, 3 of gastric carcinoid(33%) and 2 of rectal carcinoid(14%). Primary tumor size ranged from 1 to 7 cm. Tumor necrosis and endolymphatic tumor emboli were found in 57% and 43% of the metastatic carcinoids, respectively. PCNA index showed a borderline significant difference between metastatic and nonmetastatic groups(P value=0.063). The low prevalence of appendiceal carcinoid and the relatively high prevalence of gastric-rectal carcinoid may reflect a low chance of incidental appendectomy and frequent detection of gastrointestinal endoscopy.

Case Report

Primary Necrotizing Granulomatous Vasculitis of the Stomach.: Myeong Cherl Kook, Sang Yong Song, Yong Il Kim, In Sung Song, Keun Wook Lee; Korean J Pathol. 1997;31(1):68-74.

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Abstract PDF: A 55-year-old woman suffered from upper abdominal pain for two months and remained refractile against the anti-ulcer regimen. The palliative gastrectomy specimen revealed multiple shallow ulcerations on the thickened mucosal folds mainly in the antrum and body along the greater curvature where multiple, whitish nodules were found in the submucosa. Microscopically, individual submucosal nodules clearly corresponded to the necrotizing granulomatous vasculitis which were featured with diffuse fibrinoid necrosis of arterial walls accompanying granuloma formation and heavy infiltration of neutrophils, eosinophils, histiocytes and giant cells. Similar vasculitic lesions involved venules and arterioles. There were scattered vasculitic changes in the liver biopsy specimens and omentum. There were no clinical presentations or serological support of systemic involvement including systemic lupus erythematosus, Henoch-Schoenlein purpura, cryoglobulinemia or Churg-Strauss granulomatous vasculitis. We conclude that this is a hitherto undescribed primary necrotizing granulomatous vasculitis predominantly involving the stomach.

Original Article

Grading System for Gastric Epithelial Proliferative Diseases Standardized Guidelines proposed by Korean Study Group for Pathology of Digestive Diseases.: Hoguen Kim, So Young Jin, Ja June Jang, Woo Ho Kim, Sang Yong Song, Kyu Rae Kim, Eun Sil Yu, Hyung Sik Shin, Han Kyeom Kim, Jin Hee Sohn, Eun Kyung Hong, Youn Wha Kim, Jin Sook Jeong, Chang Jin Kim, Shin Eun Choi, In Suh Park, Chan Il Park, Yong Il Kim; Korean J Pathol. 1997;31(5):389-400.

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Abstract PDF: The assessment of epithelial changes in gastric mucosal biopsies has been one of the major problems caused by inconsistencies in and disagreements about nomenclature and interpretation. To resolve these issues, members of the Study Group for Pathology of Digestive Diseases reviewed microslides of 50 gastric lesions showing varying degrees of mucosal abnormality and reached the following consensus; 1) the proliferating gastric epithelium can be divided into hyperplastic and neoplastic; 2) the term "dysplasia" is reserved for the microscopic epithelial changes that are unequivocally neoplastic; 3) Biopsy specimens can be categorized as regenerative(negative for dysplasia), indefinite(questionable dysplasia), positive(positive for dysplasia) and overt carcinoma; 4) The positive category can be divided into two subgroups, high grade dysplasia and low grade dysplasia. Criteria for each grade are presented and discussed. We offer these guidelines for establishing the correct diagnosis of the gastric mucosal biopsy specimens and for prospective studies.

Case Report

Primitive Neuroectodermal Tumor of the Kidney: A case report .: Sang Yong Song, Eun Youn Cho, Jung Won Lee, Jai Hyang Go, Mi Kyung Kim, Dae Shick Kim, Young Hyeh Ko; Korean J Pathol. 1998;32(3):231-236.

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Abstract PDF: Peripheral primitive neuroectodermal tumor (pPNET), a rare, highly aggressive neoplasm of indetermined histogenesis, occurs typically in the soft tissues of the chest wall and the paraspinal region. Comprehensive diagnostic studies including histological, ultrastructural, immunohistochemical and molecular analyses have been stressed to diagnose this entity. We report a case of primary renal PNET which was incidentally found in a 59-year-old man who presented with generalized weakness for 4 months. He was diagnosed as a non-insulin dependent diabetes mellitus 15 years ago and has been made well by oral therapy. An ill-defined mass, measuring 3.5 3 cm, located in the left kidney and perirenal fat, was incidentally found by ultrasonogram during a renal diabetic examination. The mass was resected because of the unresponsiveness against one-year chemotherapy and radiation therapy. Grossly, a homogeneously solid, gray-white mass, measuring 2.8 1.8 cm, was noted in the mid portion of renal cortex. The mass showed severe adhesion to the perirenal fatty tissue. Microscopically, tumor cells were rather uniform, small round with scanty cytoplasm and often showed rosette formation. Ultrastructurally, they showed membrane-bound dense core granules, measuring 125~150 nm, intercellular junctions and microvillous cytoplasmic projections. The tumor cells were uniformly immunoreactive for neuron-specific enolase and were focally immunoreactive for CD99 (013), chromogranin, synaptophysin and cytokeratin. They were not reactive for S-100 protein, vimentin, Leu-7, leukocyte common antigen, desmin and smooth muscle actin. To our knowledge, this is the smallest renal PNET in literature.

Original Articles

Cyclin D1 Expression in 101 Cases of Breast Carcinoma.: Duck Hwan Kim, Eun Sook Nam, Hyung Sik Shin, Jin Woo Ryu, Jai Hyang Go, Young Lyun Oh, Sang Yong Song, Dae Shick Kim, Min Chul Lee; Korean J Pathol. 1998;32(4):266-272.

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Abstract PDF: Cyclin D1, a cell cycle regulator essential for G1 phase progression, is a candidate proto-oncogene implicated in pathogenesis of several human carcinomas including breast carcinoma. We studied the cyclin D1 expression in 101 cases of primary breast carcinoma tissues. The overexpression of cyclin D1 was immunohistochemically demonstrated in 34 (37.8%) of 90 cases of invasive breast carcinoma. Positive cyclin D1 staining was seen in 32 of 79 invasive ductal carcinomas, and 2 of 3 mucinous carcinomas. All 5 medullary carcinomas, 2 invasive lobular carcinomas, and 1 metaplastic carcinoma were negative. Cyclin D1 overexpression was observed in 9 of 11 ductal carcinoma in situ (DCIS). Normal epithelial components, either ductal or lobular, were not immunoreactive for cyclin D1. No significant correlations were observed between cyclin D1 immunoreactivity and other parameters including tumor size, clinical stage, nuclear or histologic grades, lymphatic or angioinvasion, lymph node metastasis, and immunohistochemical status of progesterone receptor, p53 and c-erbB-2. The overexpression of cyclin D1 was positively correlated with estrogen receptor status (p=0.025). Based on our results, the cyclin D1 protein aberration may play a role in tumorigenesis of breast carcinoma, but does not seem to have prognostic value in invasive breast carcinoma without hormonal treatment.

Primary Central Nervous System Lymphomas; A Clinicopathologic Study of 18 Cases.: Yu Kyung Jeong, Young Hyeh Ko, Dong Kyu Na, Yeon Lim Suh, Sang Yong Song, Dae Shik Kim, Mi Kyung Kim, Howe Jung Ree; Korean J Pathol. 1998;32(9):670-679.

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Abstract: The incidence of a primary central nervous system (CNS) lymphoma in western countries is about 1% of all the intracranial tumors and has increased 2.2% over the last decade. A similar pattern of increased frequency is observed in Korea. Although most CNS lymphomas in western countries are high grade tumors carrying poor prognosis, the clinicopathologic features of the Korean CNS lymphoma have not been well studied. We report clinicopathological features of 18 cases of histologically proven primary brain lymphoma. The mean age of the patients was 50 years and there was no sex difference. The clinical and radiological characteristics included multiple site of occurrence, infrequent extracranial spread, and frequent seeding via cerebrospinal fluid. No patients were immune-compromised host. Of 18 cases, 15 cases were of B-lineage and 2 cases were of T-lineage. According to REAL classification, there were 12 cases of diffuse large B cell lymphoma, two cases of B cell lymphomas of small lymphoid cell, and two cases of peripheral T cell lymphoma, unspecified. The remaining subtypes were not subclassified because of inadequate material. Pleomorphic cytologic features and necrosis of varying extent were frequent in the cases of diffuse large B-cell lymphoma. These results suggest that overall clinicopathologic features of primary malignant lymphomas of the central nervous system in Korea are similar to those of western countries.

Significance of the Expression of Cyclin-Dependent Kinase Inhibitor, p27Kip1, in Human Breast Cancer.: Sang Yong Song, Duck Hwan Kim, Yeon Lim Suh, Young Hyeh Ko, Dae Shick Kim, Seok Jin Nam, Jung Hyun Yang; Korean J Pathol. 1998;32(12):1081-1088.

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Abstract: p27Kip1 protein, a negative cell cycle regulator in G1 progression, has been reported to be related with human cancers including colon, breast and non-small cell lung carcinomas. To elucidate a possible prognostic indicator, we studied 49 cases of human breast carcinoma for expression of p27Kip1 protein using an immunohistochemical method, and compared these results with known prognostic parameters of the breast cancer. p27Kip1 protein was intensely stained in nuclei of carcinoma cells in 26 cases (53.1%). The expression rate of p27Kip1 protein was significantly higher in higher nuclear grade (p<0.05), lower histologic grade (p<0.01), lower N classification (p<0.001) and lower clinical stage (p<0.05) than in lower nuclear grade, higher histologic grade, higher N classification and higher clinical stage, respectively. p27Kip1 protein expression was significantly correlated with progesterone receptor status (p<0.05) or cyclin D expression (p<0.05). No statistical correlations were found between expression of p27Kip1 protein and other parameters including tumor size, estrogen receptor status, p53 overexpression and c-erbB-2 expression. The results suggest that reduced expression of p27Kip1 protein plays a role in biologically aggressive behavior of breast carcinoma and might contribute in predicting breast cancer patient's survival.

Case Report

Sex Cord Tumor with Annular Tubules and Serous Surface Papillary Carcinoma of the Ovary: A case report.: Dae su Kim, Sang Yong Song, Geung hwan Ahn; Korean J Pathol. 1999;33(8):627-630.

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Abstract PDF: Sex cord tumor with annular tubules (SCTAT) is a rare ovarian neoplasm which usually occurs in two forms. In patients associated with Peutz-Jeghers syndrome, the tumors are usually small, bilateral or multifocal, and show benign clinical course. However, tumors from patients without the syndrome are often large, usually unilateral, and rarely show malignant behavior. Serous surface papillary carcinoma (SSPC) is an aggressive neoplasm which involves peritoneal linings, including ovarian surface. Recently, we encountered a case of an unusual combination of SCTAT and SSPC in the ovary of a 55-year-old Korean woman presented with abdominal distention for one year. Systemic review and physical examination were within normal limit, except for abdominal discomfort and distention. There was no stigmata of Peutz-Jeghers syndrome in all diagnostic examinations, including gastroscopy and colonoscopy. Pelvic computed tomography showed adnexal mass with multiple peritoneal nodules. Exploration revealed uterine and ovarian surfaces covered with multiple, yellow-white papillary nodules. However, the sizes of both ovaries were within normal limit. Typical serous papillary carcinomas were identified in nodules from peritoneum and ovarian surfaces. Well-circumscribed columnar epithelial cell nests composed of ring-shaped tubules encircling hyalinized basement membrane-like materials were found in the ovary away from serous surface papillary carcinoma.

Original Articles

Expression of p27kip1, Cyclin D1 and p53 Protein in Ductal Carcinoma In Situ of the Breast.: Young Lyun Oh, Sang Yong Song, Jong Sun Choi, Young Hyeh Ko, Hwoe J Ree, Geung Hwan Ahn; Korean J Pathol. 1999;33(9):709-716.

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Abstract PDF: p27(kip1) protein, a cyclin-dependent kinase inhibitor, has been reported to be a powerful negative prognostic marker in patients with breast carcinoma. However, to this day, studies on p27(kip1) protein expression in ductal carcinoma in situ (DCIS) have been extremely limited. We studied the immunohistochemical expression of p27(kip1) protein in 49 cases of the DCIS and compared the findings to the clinicopathologic parameters, cyclin D1, p53 and estrogen receptor (ER). Positive nuclear staining of p27(kip1) protein was identified in 23 (46.9%) cases. The p27(kip1) protein expression correlated positively with the cyclin D1 immunopositivity (p<0.005) and ER expression (p<0.005). No significant associations were seen in the p27(kip1) protein expression and clinicopathologic parameters. The overexpression of cyclin D1 (59.2% of the cases) correlated positively with ER expression (p<0.001). The p53 protein expression was identified in 30.6% and seemed to be correlated inversely with ER expression (p=0.06). The DCISs with high grade nuclei were more likely to be p53-positive (p<0.05). Our data suggest that the expression of p27(kip1) protein as well as cyclin D1 and p53 protein may be influenced by the ER status in DCIS. The significantly positive correlation of p27(kip1) protein and cyclin D1 expression (p<0.005) supports the theory that the balance of the two opposing signals is important in determining the cell proliferation in breast cancers. Therefore, a comprehensive understanding of loop reaction of p27(kip1)-cyclin D1-ER may be necessary for the treatment of DCIS.

Quality Assurance of Frozen Section Diagnosis An analysis of 5,273 consecutive cases .: Sang Yong Song, Geunghwan Ahn; Korean J Pathol. 1999;33(12):1182-1190.

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Abstract PDF: Quality assurance analysis of frozen section diagnosis is very important for the pathologists to improve the diagnostic ability and the quality of medical service. We analysed 5,273 consecutive cases of frozen section diagnosis which were done in Samsung Medical Center during 10 months from June 1, 1998 to March 31. 1999 with special reference to the discordance between frozen section diagnosis and final diagnosis. The concordance rate was 97.65%, discordance rate 1.34%, and deferred diagnosis (type 1) rate 1.01%. Category A (discordant diagnosis without any effect on the patients) was 53 cases (1.01%), category B (discordant diagnosis with minimal but no serious effect on the patients) was 10 cases (0.19%), and category C (discordant diagnosis with serious effect on the patients) was 8 cases (0.15%). Type 2 (discordant diagnosis by extra-pathologist problem) was 22 cases (0.42%) and type 3 (discordant diagnosis by pathologist problem) was 49 cases (0.93%). The most frequent causes of type 2 and 3 discordant diagnosis were presence of new lesions on deeper sections and the misinterpretation of lesions. Discordant diagnosis was noted in lymphoreticular system, central nervous system, thyroid, gastric resection margin, breast, female genital organs, intestine, hepatobiliary system, upper aerodigestive tract, urinary tract, lung, and soft tissue in descending order of frequency. Frozen section diagnosis was deferred in central nervous system, lymphoreticular system, gastric resection margin, female genital organs, thyroid, intestine, upper aerodigestive tract, lung, and soft tissue in descending order of frequency. The most important cause of discordant diagnosis was a misinterpretation of the lesions. Based on our results, a continuous and careful follow-up of quality assurance analysis of frozen section diagnosis and a share of experience of problematic cases are mandatory for the pathologists to improve the quality of medical services.

Pathologic Characteristics of Korean Prostatic Adenocarcinoma: A Mapping Analysis of 60 Cases.: Yoon La Choi, Sung Rim Kim, Sang Yong Song, Han Yong Choi; Korean J Pathol. 2001;35(1):35-40.

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Abstract PDF: BACKGROUND
Pathologic characteristics of the prostatic adenocarcinoma in Korean patients are not clear. We studied 60 cases of radical prostatectomy specimens using mapping analysis in an effort to discover the pathologic characteristics of the Korean prostatic adenocarcinoma.
METHODS
A resected prostate was sectioned serially and embedded near-totally. Gleason score, tumor volume or size, capsular extension, involvement of lateral margin, seminal vesicle, vas, apex and base, presence of lymphatic and neural invasion, and presence of high grade prostatic intraepithelial neoplasm (HGPIN) were examined. DNA ploidy and proliferative index were evaluated.
RESULTS
Mean values were as follows: age, 63.6 years; serum prostate specific antigen level (sPSA), 24.0 ng/ml; tumor amount (volume, 29.1%; size, 2.4 cm); Gleason score, 7.3; aneuploidy, 23.3%; proliferative index, 14.2%. Involvement rates of apex, base, seminal vesicle, resection margin, nerve and lymphatics were 5.2%, 39.0%, 23.7%, 31.7%, 56.7% and 16.7%, respectively. Rates of multifocal tumors and HGPIN were 43.3% and 63.3%, respectively. The Gleason score was correlated with tumor amount (volume%, p<0.001; size, p<0.01) and tumor extent (T) (p<0.005). Tumor amount was correlated with sPSA (p<0.05) and T (p<0.005). T was correlated with sPSA (p<0.05).
CONCLUSION
Korean prostatic adenocarcinomas showed higher Gleason scores, lower HGPIN rates and multifocalities in comparison to western prostatic adenocarcinomas, suggestive of the Korean prostatic adenocarcinomas' late detection.

Case Report

Atypical (Bizarre) Leiomyoma of the Prostate: A Case Report.: Sung Rim Kim, Sang Yong Song, Geunghwan Ahn, Han Yong Choi; Korean J Pathol. 2001;35(2):172-175.

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Abstract PDF: Atypical (bizarre) leiomyoma of the prostate is a very rare neoplasm. Five cases have been reported in English medical literature. A 60-year-old Korean man with a history of prostatism and slightly elevated serum prostate specific antigen was presented. Microscopically, the transurethral resection specimen consisted of a proliferation of hypercellular spindle cells with intersecting bundles. The nuclei of the tumor cells showed marked pleomorphism and hyperchromasia with occasional multinucleated giant cells. Mitoses were seen in areas of up to 2 per 10 high power fields, but there was no evidence of atypical ones. The tumor cells were immunoreactive against anti-smooth muscle actin and desmin antibodies. The proliferative index (10.0%) of the atypical leiomyoma lay between that of a benign smooth muscle and that of a leiomyosarcoma of the prostate. Flow cytometry showed a diploid pattern with an elevated S phase fraction. To the best of our knowledge, this is the first demonstration of atypical leiomyoma of the prostate in a Korean man.

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