Journal of Pathology and Translational Medicine

Case Study

Malignant potential of neuroendocrine microtumor of the pancreas harboring high-grade transformation: lesson learned from a patient with von Hippel-Lindau syndrome: Jongwon Lee, Kyung Jin Lee, Dae Wook Hwang, Seung-Mo Hong; J Pathol Transl Med. 2024;58(2):91-97. Published online March 13, 2024; DOI: https://doi.org/10.4132/jptm.2024.02.13

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Abstract PDF: Pancreatic neuroendocrine microtumor (PNEMT) is a neuroendocrine tumor (NET) < 0.5 cm in diameter, and it is considered benign. We report a PNEMT with high-grade transformation (HGT). A man in his 60s with von Hippel-Lindau syndrome underwent surgical resection of a NET. A second sub-centimeter nodule with a nodule-in-nodule pattern was discovered. The 0.4 cm outer nodule contained clear columnar cells with round nuclei and indistinct nucleoli, while the 0.1 cm inner nodule had eosinophilic cells with an increased nuclear to cytoplasmic ratio, vesicular nuclei, and prominent nucleoli. Tumor cells in the outer and inner nodules were synaptophysin and chromogranin positive. Only the inner nodule was p53 positive, while the outer nodule was exclusively positive for carbonic anhydrase 9 and vimentin. The Ki-67 labeling indices for the outer and inner nodules were 2.1% (grade 1) and 44.3% (grade 3), respectively. This nodule was determined to be a PNEMT with HGT. Our findings suggest that a PNEMT may not always be benign and can undergo HGT.

Original Articles

Lymph node size and its association with nodal metastasis in ductal adenocarcinoma of the pancreas: Jaehoon Shin, Seungbeom Shin, Jae Hoon Lee, Ki Byung Song, Dae Wook Hwang, Hyoung Jung Kim, Jae Ho Byun, HyungJun Cho, Song Cheol Kim, Seung-Mo Hong; J Pathol Transl Med. 2020;54(5):387-395. Published online July 21, 2020; DOI: https://doi.org/10.4132/jptm.2020.06.23

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Background
Although lymph node metastasis is a poor prognostic factor in patients with pancreatic ductal adenocarcinoma (PDAC), our understanding of lymph node size in association with PDAC is limited. Increased nodal size in preoperative imaging has been used to detect node metastasis. We evaluated whether lymph node size can be used as a surrogate preoperative marker of lymph node metastasis.
Methods
We assessed nodal size and compared it to the nodal metastatic status of 200 patients with surgically resected PDAC. The size of all lymph nodes and metastatic nodal foci were measured along the long and short axis, and the relationships between nodal size and metastatic status were compared at six cutoff points.
Results
A total of 4,525 lymph nodes were examined, 9.1% of which were metastatic. The mean size of the metastatic nodes (long axis, 6.9±5.0 mm; short axis, 4.3±3.1 mm) was significantly larger than that of the non-metastatic nodes (long axis, 5.0±4.0 mm; short axis, 3.0±2.0 mm; all p<.001). Using a 10 mm cutoff, the sensitivity, specificity, positive predictive value, overall accuracy, and area under curve was 24.8%, 88.0%, 17.1%, 82.3%, and 0.60 for the long axis and 7.0%, 99.0%, 40.3%, 90.6%, and 0.61 for the short axis, respectively.
Conclusions
The metastatic nodes are larger than the non-metastatic nodes in PDAC patients. However, the difference in nodal size was too small to be identified with preoperative imaging. The performance of preoperative radiologic imaging to predict lymph nodal metastasis was not good. Therefore, nodal size cannot be used a surrogate preoperative marker of lymph node metastasis.

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Does direct invasion of peripancreatic lymph nodes impact survival in patients with pancreatic ductal adenocarcinoma? A retrospective dual-center study
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CA19.9 Serum Level Predicts Lymph-Nodes Status in Resectable Pancreatic Ductal Adenocarcinoma: A Retrospective Single-Center Analysis
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Sarcoma metastasis to the pancreas: experience at a single institution: Miseon Lee, Joon Seon Song, Seung-Mo Hong, Se Jin Jang, Jihun Kim, Ki Byung Song, Jae Hoon Lee, Kyung-Ja Cho; J Pathol Transl Med. 2020;54(3):220-227. Published online April 22, 2020; DOI: https://doi.org/10.4132/jptm.2020.03.04

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Abstract PDF

Background
Reports of metastatic sarcoma to the pancreas are limited. We reviewed the clinicopathologic characteristics of such cases.
Methods
We reviewed 124 cases of metastatic tumors to the pancreas diagnosed at Asan Medical Center between 2000 and 2017.
Results
Metastatic tumors to the pancreas consisted of 111 carcinomas (89.5%), 12 sarcomas (9.6%), and one melanoma (0.8%). Primary sarcoma sites were bone (n = 4); brain, lung, and soft tissue (n = 2 for each); and the uterus and pulmonary vein (n = 1 for each). Pathologically, the 12 sarcomas comprised 2 World Health Organization grade III solitary fibrous tumors/hemangiopericytomas, and one case each of synovial sarcoma, malignant solitary fibrous tumor, undifferentiated pleomorphic sarcoma, osteosarcoma, mesenchymal chondrosarcoma, intimal sarcoma, myxofibrosarcoma, myxoid liposarcoma, rhabdomyosarcoma, subtype uncertain, and high-grade spindle-cell sarcoma of uncertain type. The median interval between primary cancer diagnosis and pancreatic metastasis was 28.5 months. One case manifested as a solitary pancreatic osteosarcoma metastasis 15 months prior to detection of osteosarcoma in the femur and was initially misdiagnosed as sarcomatoid carcinoma of the pancreas.
Conclusions
The metastatic sarcoma should remain a differential diagnosis when spindle-cell malignancy is found in the pancreas, even for solitary lesions or in patients without prior history.

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Case Study

Coexisting Mucinous Cystic Neoplasm of the Pancreas and Type 1 Autoimmune Pancreatitis: Mee-Jeong Kim, Tae Jun Song, Hyoung Jung Kim, Song-Cheol Kim, Myung-Hwan Kim, Seung-Mo Hong; J Pathol Transl Med. 2019;53(2):125-128. Published online November 14, 2018; DOI: https://doi.org/10.4132/jptm.2018.10.25

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Abstract PDF

Type 1 autoimmune pancreatitis (AIP1) is an IgG4-related systemic disease that mimics tumors. We report a rare case of AIP1 accompanied by mucinous cystic neoplasm (MCN). A pancreatic lesion was incidentally detected in a woman in her 60s. After 6 years of follow-up, the lesion abruptly increased in size. Computed tomography showed a 3.5 cm unilocular cyst in the tail of the pancreas and distal pancreatectomy was performed. On microscopic examination, the cyst was lined by mucinous and non-mucinous epithelial cells with mild cytologic atypia. The surrounding stroma comprised ovarian-type spindle cells with progesterone receptor positivity. The pericystic pancreas exhibited multifocal lymphoid follicles, lymphoplasmacytic infiltrations, obliterative phlebitis, and storiform fibrosis. IgG4-positive plasma cell infiltration (215 cells high-power field) and the IgG4/IgG ratio (57%) were increased. Cases of MCN coexisting with AIP1 are extremely rare; only two such cases have been reported in the English-language literature. This third case featured low-grade MCN with AIP1.

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Histological features of autoimmune pancreatitis and IgG4-related sclerosing cholangitis with a correlation with imaging findings
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Choonpa Igaku.2023; 50(1): 55. CrossRef
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Original Article

Loss of Progesterone Receptor Expression Is an Early Tumorigenesis Event Associated with Tumor Progression and Shorter Survival in Pancreatic Neuroendocrine Tumor Patients: Sung Joo Kim, Soyeon An, Jae Hoon Lee, Joo Young Kim, Ki-Byung Song, Dae Wook Hwang, Song Cheol Kim, Eunsil Yu, Seung-Mo Hong; J Pathol Transl Med. 2017;51(4):388-395. Published online June 8, 2017; DOI: https://doi.org/10.4132/jptm.2017.03.19

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Abstract PDF

Background
Pancreatic neuroendocrine tumors (PanNETs) are the second most common pancreatic neoplasms and there is no well-elucidated biomarker to stratify their detection and prognosis. Previous studies have reported that progesterone receptor (PR) expression status was associated with poorer survival in PanNET patients.
Methods
To validate previous studies, PR protein expression was assessed in 21 neuroendocrine microadenomas and 277 PanNETs and compared with clinicopathologic factors including patient survival.
Results
PR expression was gradually decreased from normal islets (49/49 cases, 100%) to neuroendocrine microadenoma (14/21, 66.6%) to PanNETs (60/277, 21.3%; p < .001). PanNETs with loss of PR expression were associated with increased tumor size (p < .001), World Health Organization grade (p = .001), pT classification (p < .001), perineural invasion (p = .028), lymph node metastasis (p = .004), activation of alternative lengthening of telomeres (p = .005), other peptide hormonal expression (p < .001) and ATRX/DAXX expression (p = .015). PanNET patients with loss of PR expression (5-year survival rate, 64.1%) had significantly poorer recurrence-free survival outcomes than those with intact PR expression (90%) by univariate (p = .012) but not multivariate analyses. Similarly, PanNET patients with PR expression loss (5-year survival rate, 76%) had significantly poorer overall survival by univariate (p = .015) but not multivariate analyses.
Conclusions
Loss of PR expression was noted in neuroendocrine microadenomas and was observed in the majority of PanNETs. This was associated with increased grade, tumor size, and advanced pT and pN classification; and was correlated with decreased patient survival time by univariate but not multivariate analyses. Loss of PR expression can provide additional information on shorter disease-free survival in PanNET patients.

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Venous invasion and lymphatic invasion are correlated with the postoperative prognosis of pancreatic neuroendocrine neoplasm
Sho Kiritani, Junichi Arita, Yuichiro Mihara, Rihito Nagata, Akihiko Ichida, Yoshikuni Kawaguchi, Takeaki Ishizawa, Nobuhisa Akamatsu, Junichi Kaneko, Kiyoshi Hasegawa
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Combined Infiltrative Macroscopic Growth Pattern and Infiltrative Microscopic Tumor Border Status Is a Novel Surrogate Marker of Poor Prognosis in Patients With Pancreatic Neuroendocrine Tumor
Bokyung Ahn, Joo Young Kim, Seung-Mo Hong
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HORMONET: a phase II trial of tamoxifen for estrogen/progesterone receptor-positive neuroendocrine tumors
Milton J. Barros, Jonathan Strosberg, Taymeyah Al-Toubah, Victor Hugo F. de Jesus, Lais Durant, Celso A. Mello, Tiago C. Felismino, Louise De Brot, Rodrigo G. Taboada, Mauro D. Donadio, Rachel P. Riechelmann
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Review

Cytology Specimen Management, Triage and Standardized Reporting of Fine Needle Aspiration Biopsies of the Pancreas: Won Jae Yoon, Martha Bishop Pitman; J Pathol Transl Med. 2015;49(5):364-372. Published online August 10, 2015; DOI: https://doi.org/10.4132/jptm.2015.07.19

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Abstract PDF

The recent advances in pancreas cytology specimen sampling methods have enabled a specific cytologic diagnosis in most cases. Proper triage and processing of the cytologic specimen is pivotal in making a diagnosis due to the need for ancillary testing in addition to cytological evaluation, which is especially true in the diagnosis of pancreatic cysts. Newly proposed terminology for pancreaticobiliary cytology offers a standardized language for reporting that aims to improve communication among patient caregivers and provide for increased flexibility in patient management. This review focuses on these updates in pancreas cytology for the optimal evaluation of solid and cystic lesions of the pancreas.

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Original Articles

Diagnostic Accuracy of Endoscopic Ultrasound-Guided Fine Needle Aspiration Cytology of Pancreatic Lesions: Hae Woon Baek, Min Jee Park, Ye-Young Rhee, Kyoung Bun Lee, Min A Kim, In Ae Park; J Pathol Transl Med. 2015;49(1):52-60. Published online January 15, 2015; DOI: https://doi.org/10.4132/jptm.2014.10.26

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Abstract PDF

Background
Endoscopic ultrasound–guided fine needle aspiration cytology (EUS-FNAC) is currently the most commonly used procedure for obtaining cytologic specimens of the pancreas. It is accurate, minimally invasive, safe and cost-effective. However, there is discrepancy between cytological and surgical diagnoses. This study was aimed at evaluating the diagnostic accuracy of EUS-FNAC of the pancreas. Methods: We performed a retrospective review of 191 cases of pancreatic lesions initially diagnosed by EUS-FNAC with subsequent histological diagnosis between 2010 and 2012 in the Department of Pathology, Seoul National University Hospital. Cytologic and surgical diagnoses were categorized into five groups: negative, benign, atypical, malignant, and insufficient for diagnosis. Subsequently, 167 cases with satisfactory yield in both surgical and cytology specimens were statistically analyzed to determine correlations with diagnosis. Results: In comparison to surgical diagnoses, cytologic diagnoses were true-positive in 103 cases (61.7%), true-negative in 28 cases (16.8%), false-positive in 9 cases (5.4%), and false-negative in 27 cases (16.1%). The diagnostic accuracy was 78.4%, sensitivity was 79.2%, and specificity was 75.7%. The positive predictive value was 92.0%, and negative predictive value was 50.9%. Conclusions: EUS-FNAC has high accuracy, sensitivity, specificity and positive predictive value. Overcoming the limitations of EUS-FNAC will make it a useful and reliable diagnostic tool for accurate evaluation of pancreatic lesions.

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It is necessary to exam bottom and top slide smears of EUS-FNA for pancreatic cancer
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Clinical and Prognostic Significances of Cytokeratin 19 and KIT Expression in Surgically Resectable Pancreatic Neuroendocrine Tumors: Eun-Mi Son, Joo Young Kim, Soyeon An, Ki-Byung Song, Song Cheol Kim, Eunsil Yu, Seung-Mo Hong; J Pathol Transl Med. 2015;49(1):30-36. Published online January 15, 2015; DOI: https://doi.org/10.4132/jptm.2014.10.23

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Abstract PDF

Background
Pancreatic neuroendocrine tumors (PanNETs) are malignant endocrine neoplasms that present diverse clinical behaviors. Therefore, identification of biomarkers of PanNETs is important for stratification of the prognosis of PanNET patients. Recently, cytokeratin 19 (CK19) and KIT expression were reported to have prognostic significance in PanNET patients. Methods: To identify their prognostic significance, CK19 and KIT protein expression were assessed in 182 surgically resected PanNETs and compared with clinicopathologic factors. Results: Of 182 PanNETs cases, CK19 and KIT expression was noted in 97 (53.3%) and 16 (8.8%) cases, respectively. PanNET patients with CK19 expression had larger tumors (p=.006), higher World Health Organization (WHO) grade (p=.002) and pT classification (p<.001), increased distant metastasis (p=.004), and lymphovascular (p=.012) and perineural (p=.019) invasion. Similarly, those with KIT expression had larger tumors (p=.030), higher WHO grade (p=.001), advanced pT classification (p<.001), distant metastasis (p=.001), and lymphovascular invasion (p=.014). The 5-year survival rate for PanNET patients with KIT expression was significantly lower (62%) than that of patients without KIT expression (77%, p=.011), as determined by univariate but not by multivariate analyses. Conclusions: CK19 and KIT expression correlate with higher metastatic potential and advanced disease stage, and KIT expression is associated with worse survival in PanNET patients.

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Brief Case Report

Pulmonary Hodgkin Lymphoma in a Patient with Crohn’s Disease: Jae-Young Park, Juhie Lee; Korean J Pathol. 2014;48(5):387-389. Published online October 27, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.5.387

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Review & Perspective

Acinar Cell Carcinoma of the Pancreas: Clinical and Cytomorphologic Characteristics: Adam D. Toll, Ralph H. Hruban, Syed Z. Ali; Korean J Pathol. 2013;47(2):93-99. Published online April 24, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.2.93

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Abstract PDF

Acinar cell carcinoma is a rare malignant epithelial neoplasm with predominantly exocrine acinar differentiation and is seen primarily in older men (mean age, 62 years). The presenting symptoms are usually non-specific, and jaundice is often not present. Symptoms relating to the overproduction and release of lipase into the circulation are present in 10-15% of patients. Characteristic cytomorphologic features include a population of cells with minimal pleomorphism, eccentrically placed nuclei with a single prominent nucleoli and moderate hyperchromasia. The cytoplasm is finely granular, and the background may contain granular debris secondary to cytolysis. A significant proportion of the cases also have a minor neuroendocrine component or scattered neuroendocrine cells. Approximately 50% of patients have metastatic disease at presentation, often restricted to the regional lymph nodes and liver. The prognosis is poor, only slightly better than that of pancreatic ductal adenocarcinoma.

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Case Report

Adenocarcinoma with Intraductal Papillary Mucinous Neoplasm Arising in Jejunal Heterotopic Pancreas: Ju Young Song, Jee Young Han, Sun Keun Choi, Lucia Kim, Suk Jin Choi, In Suh Park, Young Chae Chu, Kyu Ho Kim, Joon Mee Kim; Korean J Pathol. 2012;46(1):96-100. Published online February 23, 2012; DOI: https://doi.org/10.4132/KoreanJPathol.2012.46.1.96

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Abstract PDF

A 74-year-old man suffered from jejunal perforation and adhesion to sigmoid colon due to adenocarcinoma associated with intraductal papillary mucinous neoplasm (IPMN) arising in a jejunal heterotopic pancreas. The jejunal lesion showed direct extension to the sigmoid colon, which was mistaken as sigmoid colon cancer by surgeons. Malignant transformation is a rare complication of a heterotopic pancreas. About half of malignancies in reported cases were ductal adenocarcinoma arising in the stomach, and the jejunal location is extremely rare. Furthermore, IPMN is also uncommon finding in a heterotopic pancreas.

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Original Article

Fine Needle Aspiration Cytology of Solid and papillary Neoplasm of the Pancreas: Report of a Case.: Mee Yon Cho, Kwang Gil Lee, Kyi Beom Lee, Hyeun Joo Jeong, Woo Hee Jung; Korean J Cytopathol. 1990;1(1):85-92.

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Abstract PDF: We present the cytologic features of a case of solid and papillary neoplasm of the pancreas. Cytologically, the tumor was composed of a monotonous population of polygonal cells containing ecentrically located round nuclei with one or two distinct small nucleoli and a finely stippled chromatin pattern. The tumor cells were similar to those of the islet cell tumor and showed isolated loosety aggregated and solid sheedts or large cell clumps. The large cell clumps revealed a branching papillary structure containing fibrovascular central core, which is characteristic histologic feature of solid and papillary neoplasm of the pancreas. The case was confirmed by tissue examination including histochemical immunohistochemical and electron microscopical studies. Utrastructurally, the tumor cells contanined a few membrane-bound electron dense granules.

Case Report

Simultaneous Pancreatic Serous Microcystic Adenoma and Intraductal Papillary Mucinous Tumor of the Pancreas: A Case Report.: Hyoung Jong Kwak, Young Kon Kim, Baik Hwan Cho, Woo Sung Moon; Korean J Pathol. 2011;45:S29-S31.; DOI: https://doi.org/10.4132/KoreanJPathol.2011.45.S1.S29

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Abstract PDF: Serous cystadenomas of the pancreas account for approximately a third of pancreatic cystic neoplasms. Their coexistence with a second tumor is extremely rare. We now report a case of a serous microcystic adenoma combined with an intraductal papillary mucinous tumor of the pancreas in a 69-year-old man. Abdominal computed tomography scans demonstrated an incidental cystic mass in the body with cystic dilatation of the duct in the head of the pancreas. Central pancreatectomy with pancreatico-jejunostomy, and cyst excision of the pancreatic head were performed. Histologic examination demonstrated a serous microcystic cystadenoma in the body coexisting with an intraductal papillary mucinous adenoma in the head of the pancreas. This case study highlights the importance of careful intra-operative and pathologic examination for synchronous pancreatic tumors.

Original Article

Clinical Outcome of Surgically Resected Pancreatic Intraductal Papillary Mucinous Neoplasm According to the Marginal Status: A Single Center Experience.: Sun A Kim, Eunsil Yu, Song Cheol Kim, Jihun Kim; Korean J Pathol. 2010;44(4):410-419.; DOI: https://doi.org/10.4132/KoreanJPathol.2010.44.4.410

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Abstract PDF

BACKGROUND
Surgical resection is the treatment of choice of intraductal papillary mucinous neoplasm (IPMN) of the pancreas. However, the benefit of clearing resection margin is still controversial.
METHODS
We reviewed 281 surgically resected cases of IPMN. The recurrences were compared according to the histologic grade (benign or borderline IPMN, malignant noninvasive IPMN, invasive carcinoma) and size (pancreatic intraepithelial neoplasia, PanIN, less than 0.5 cm in the long axis; and IPMN, greater than or equal to 0.5 cm) of the residual lesions at the resection margin.
RESULTS
Sixty cases (21.4%) were invasive carcinoma, and 221 (78.6%) noninvasive cases included 87 (31.0%) benign, 107 (38.1%) borderline and 11 (3.9%) malignant noninvasive IPMN cases. In noninvasive IPMN, increased recurrence in patients with five or more years of follow-up was only related to the involvement of resection margin by severe dysplasia. The recurrence of invasive carcinoma was high (27.3%) even when the resection margin was clear, and was not related to the grade or size of residual tumors at the resection margin.
CONCLUSIONS
Invasiveness is a strong risk factor for recurrence in IPMN regardless of the status of the resection margin. However, in noninvasive IPMN, histologic grading of residual lesions at the resection margin predicts local recurrence.

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Systematic review of challenging issues in pathology of intraductal papillary mucinous neoplasms
Laura D. Wood, N. Volkan Adsay, Olca Basturk, Lodewijk A.A. Brosens, Noriyoshi Fukushima, Seung-Mo Hong, Sung-Joo Kim, Jae W. Lee, Claudio Luchini, Michaël Noë, Martha B. Pitman, Aldo Scarpa, Aatur D. Singhi, Mariko Tanaka, Toru Furukawa
Pancreatology.2023; 23(7): 878. CrossRef
The Use of Intraoperative Frozen Sections in Guiding the Extent of Pancreatic Resections for Intraductal Papillary Mucinous Neoplasms
Zhikai Chi, Deepti Dhall, Richard Mertens
Pancreas.2022; 51(1): 63. CrossRef
Recurrence of non-invasive intraductal papillary municious neoplasm seven years following total pancreatectomy
Nayima M. Clermont Dejean, Sinziana Dumitra, Jeffrey S. Barkun
International Journal of Surgery Case Reports.2013; 4(9): 789. CrossRef

Case Report

Intraductal Papillary Mucinous Tumor Simultaneously Involving the Liver and Pancreas: A Case Report.: Bong Hee Park, Jae Hee Suh, Hee Jeong Cha, Young Min Kim, Hye Jeong Choi; Korean J Pathol. 2010;44(1):83-86.; DOI: https://doi.org/10.4132/KoreanJPathol.2010.44.1.83

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Abstract PDF

We describe here a 67-year-old man who was diagnosed with a rare case of intraductal papillary mucinous tumors that occurred simultaneously in the liver and pancreas. Abdominal computed tomography showed a tubular and cystic dilatation of the pancreatic duct in the pancreas tail, which suggested an intraductal papillary mucinous tumor (IPMT), and multiple intrahepatic duct stones. The patient underwent a distal pancreatectomy with splenectomy and a lateral segmentectomy of the liver. Microscopic examination showed an intraductal papillary mucinous neoplasms of borderline malignancy in the pancreas and a non-invasive intraductal papillary mucinous tumor with moderate dysplasia of the bile duct. Although several cases of intraductal papillary mucinous neoplasm of the liver (IPNL) without any pancreatic association have been described, the simultaneous presentation of both IPMT of the pancreas and IPNL is very rare. The patient has been doing well for 10 months postoperatively.

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World Journal of Gastroenterology.2023; 29(38): 5361. CrossRef
Multicentric recurrence of intraductal papillary neoplasm of bile duct after spontaneous detachment of primary tumor: A case report
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World Journal of Clinical Cases.2022; 10(3): 1000. CrossRef
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World Journal of Clinical Cases.2019; 7(1): 102. CrossRef
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Clinical Imaging.2016; 40(5): 897. CrossRef

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