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      Extensively Invasive Gallbladder Cancer from Intracholecystic Papillary Neoplasm Treated with Pylorus-Preserving Pancreaticoduodenectomy and Extended Cholecystectomy: A Case Report and Literature Review

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          Abstract

          Background

          Intracholecystic papillary neoplasm (ICPN) is a rare tumor first classified by the World Health Organization in 2010. ICPN is a counterpart of the intraductal papillary mucinous neoplasm of the pancreas and intraductal papillary neoplasm of the bile duct. Previous reports on ICPN are limited; thus, the diagnosis, surgical intervention, and prognosis are controversial. Here, we report an extensively invasive gallbladder cancer arising in ICPN treated with pylorus-preserving pancreaticoduodenectomy (PPPD) and extended cholecystectomy. Case Presentation. A 75-year-old man presented to another hospital with jaundice for 1 month. Laboratory findings showed elevated total bilirubin, 10.6 mg/dL and carbohydrate antigen 19-9, 54.8 U/mL. Computed tomography showed a well-enhanced tumor located in the distal bile duct and dilated hepatic bile duct. The gallbladder wall was thickened and homogeneously enhanced. Endoscopic retrograde cholangiopancreatography revealed a filling defect in the distal common bile duct, and intraductal ultrasonography showed a papillary tumor in the common bile duct, indicating tumor invasion of the bile duct subserosa. Subsequent bile duct brush cytology revealed adenocarcinoma. The patient was referred to our hospital for surgical treatment and underwent an open PPPD. Intraoperative findings showed a thickened and indurated gallbladder wall, suggesting concurrent gallbladder cancer; thus, the patient subsequently underwent PPPD and extended cholecystectomy. Histopathological findings confirmed gallbladder carcinoma originating from ICPN, which extensively invaded the liver, common bile duct, and pancreas. The patient started adjuvant chemotherapy (tegafur/gimeracil/oteracil) 1 month after surgery and had no recurrence at follow-up after 1 year.

          Conclusions

          Accurate preoperative diagnosis of ICPN, including the extent of tumor invasion is challenging. To ensure complete curability, the development of an optimal surgical strategy considering preoperative examinations and intraoperative findings is essential.

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          Most cited references43

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          Intracholecystic papillary-tubular neoplasms (ICPN) of the gallbladder (neoplastic polyps, adenomas, and papillary neoplasms that are ≥1.0 cm): clinicopathologic and immunohistochemical analysis of 123 cases.

          Volkan Adsay, Kee-Taek Jang, Juan Carlos Roa … (2012)
          The literature on the clinicopathologic characteristics of tumoral intraepithelial neoplasms (neoplastic polyps) of the gallbladder (GB) is fairly limited, due in part to the variability in definition and terminology. Most reported adenomas (pyloric gland type and others) were microscopic and thus regarded as clinically inconsequential, whereas papillary in situ carcinomas have been largely considered a type of invasive adenocarcinoma under the heading of "papillary adenocarcinomas." In this study, 123 GB cases that have a well-defined exophytic preinvasive neoplasm measuring ≥1 cm were analyzed. The patients were predominantly female (F/M=2:1) with a mean age of 61 y and a median tumor size of 2.2 cm. Half of the patients presented with pain, and in the other half the neoplasm was detected incidentally. Other neoplasms, most being gastrointestinal tract malignancies, were present in 22% of cases. Gallstones were identified in only 20% of cases. Radiologically, almost half were diagnosed as "cancer," roughly half with polypoid tumor, and in 10% the lesion was missed. Pathologic findings: (1) The predominant configuration was papillary in 43%, tubulopapillary in 31%, tubular in 26%. (2) Each case was assigned a final lineage type on the basis of the predominant pattern (>75% of the lesion) on morphology, and supported with specific immunohistochemical cell lineage markers. The predominant cell lineage could be identified as biliary in 50% (66% of which were MUC1), gastric foveolar in 16% (all were MUC5AC), gastric pyloric in 20% (92% MUC6), intestinal in 8% (100% CK20; 75% CDX2; 50%, MUC2), and oncocytic in 6% (17% HepPar and 17% MUC6); however, 90% of cases had some amount of secondary or unclassifiable pattern and hybrid immunophenotypes. (3) Of the cases that would have qualified as "pyloric gland adenoma," 21/24 (88%) had at least focal high-grade dysplasia and 18% had associated invasive carcinoma. Conversely, 8 of 47 "papillary adenocarcinoma"-type cases displayed some foci of low-grade dysplasia, and 15/47 (32%) had no identifiable invasion. (4) Overall, 55% of the cases had an associated invasive carcinoma (pancreatobiliary type, 58; others, 10). Factors associated significantly with invasion were the extent of high-grade dysplasia, cell type (biliary or foveolar), and papilla formation. Among systematically analyzed invasive carcinomas, tumoral intraepithelial neoplasia was detected in 6.4% (39/606). (5) The 3-year actuarial survival was 90% for cases without invasion and 60% for those associated with invasion. In contrast, those associated with invasion had a far better clinical outcome compared with pancreatobiliary-type GB carcinomas (3-yr survival, 27%), and this survival advantage persisted even with stage-matched comparison. Death occurred in long-term follow-up even in a few noninvasive cases (4/55; median 73.5 mo) emphasizing the importance of long-term follow-up. In conclusion, tumoral preinvasive neoplasms (≥1 cm) in the GB are analogous to their pancreatic and biliary counterparts (biliary intraductal papillary neoplasms, pancreatic intraductal papillary mucinous neoplasms, and intraductal tubulopapillary neoplasms). They show variable cellular lineages, a spectrum of dysplasia, and a mixture of papillary or tubular growth patterns, often with significant overlap, warranting their classification under 1 unified parallel category, intracholecystic papillary-tubular neoplasm. Intracholecystic papillary-tubular neoplasms are relatively indolent neoplasia with significantly better prognosis compared with pancreatobiliary-type GB carcinomas. In contrast, even seemingly innocuous examples such as those referred to as "pyloric gland adenomas" can progress to carcinoma and be associated with invasion and fatal outcome.
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            A case of mixed adenoneuroendocrine carcinoma of the gallbladder arising from an intracystic papillary neoplasm associated with pancreaticobiliary maljunction.

            Yoshiyuki Meguro, NORIYOSHI FUKUSHIMA, Masaru Koizumi … (2014)
            A 54-year-old Japanese woman was referred with a gallbladder tumor. Based on the results of the computed tomography scan, endoscopic retrograde cholangiopancreatography, and magnetic resonance cholangiopancreatography, a mucin-producing neoplasm of the gallbladder associated with pancreaticobiliary maljunction was diagnosed. Extended cholecystectomy, extrahepatic bile duct resection, and choledochojejunostomy were performed, and she remains free of recurrence 24 months after resection. Histopathological examination revealed that the papillary component of the lesion was an intracystic papillary neoplasm with diverse characteristics of pancreaticobiliary epithelium and intestinal epithelium including mucin. In this component, most of the papillary lesion was a high-grade intraepithelial neoplasm, but also showed slight invasion into the muscular layer. The nodular component consisted of both poorly differentiated biliary type adenocarcinoma and large cell neuroendocrine carcinoma. We report a rare case of a mixed adenoneuroendocrine carcinoma arising from an intracystic papillary neoplasm associated with pancreaticobiliary maljunction. As for the histogenesis of this tumor, based on the histopathologic appearance, transdifferentiation from poorly differentiated biliary type adenocarcinoma to large cell neuroendocrine carcinoma is considered the most possible histogenesis of this tumor.
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              Gallbladder Mixed Neuroendocrine-Non-neuroendocrine Neoplasm (MiNEN) Arising in Intracholecystic Papillary Neoplasm: Clinicopathologic and Molecular Analysis of a Case and Review of the Literature.

              Amedeo Sciarra, Edoardo Missiaglia, Mounir Trimech … (2020)
              Mixed neuroendocrine-non-neuroendocrine neoplasms (MiNENs) of the gallbladder are generally composed of adenocarcinoma and neuroendocrine carcinoma (NEC). Rare cases associated with intracholecystic papillary neoplasm (ICPN) have been reported. Although recent molecular data suggest that the different components of digestive MiNENs originate from a common precursor stem cell, this aspect has been poorly investigated in gallbladder MiNENs. We describe the clinicopathologic and molecular features of a MiNEN composed of ICPN, adenocarcinoma, and NEC. A 66-year-old woman presented with severe abdominal pain. She underwent radical cholecystectomy and an intracholecystic mass was found. Histologically, it was composed of ICPN associated with adenocarcinoma and large cell neuroendocrine carcinoma (LCNEC). The three components were positive for DNA repair proteins and p53. EMA was positive in the ICPN and adenocarcinoma components, while it was negative in the LCNEC. Heterogeneous expression of Muc5AC, cytokeratin 20, and CDX2 was only observed in the ICPN component. Cytokeratin 7 was diffusely positive in both adenocarcinoma and LCNEC components, while it was heterogeneously expressed in the ICPN. The copy number variation analysis showed overlapping results between the adenocarcinoma and LCNEC components with some minor differences with the ICPN component. The three tumor components showed the same mutation profile including TP53 mutation c.700T > C (p. Tyr234His), without mutations in other 51 genes known to be frequently altered in cancer pathogenesis and growth. This finding may support the hypothesis of a monoclonal origin of the different tumor components. We have also performed a review of the literature on gallbladder MiNENs.
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                Author and article information

                Contributors
                Hideki Kumagai:
                ORCID: https://orcid.org/0000-0001-5374-9080
                Journal
                Journal ID (nlm-ta): Case Rep Surg
                Journal ID (iso-abbrev): Case Rep Surg
                Journal ID (publisher-id): CRIS
                Title: Case Reports in Surgery
                Publisher: Hindawi
                ISSN (Print): 2090-6900
                ISSN (Electronic): 2090-6919
                Publication date Collection: 2023
                Publication date (Electronic): 24 June 2023
                Volume: 2023
                Electronic Location Identifier: 5825045
                Affiliations
                1Department of Surgery, School of Medicine, Iwate Medical University, 2-1-1 Idaidori, Yahaba, Iwate 028-3695, Japan
                2Department of Molecular Diagnostic Pathology, Iwate Medical University, 2-1-1 Idaidori, Yahaba, Iwate 028-3695, Japan
                Author notes

                Academic Editor: Wei-bo Chen

                Author information
                https://orcid.org/0000-0001-5374-9080
                https://orcid.org/0000-0003-4181-7159
                Article
                DOI: 10.1155/2023/5825045
                PMC ID: 10314817
                SO-VID: fcc14b06-e6b1-4d38-9315-ec70d6aa4961
                Copyright statement: Copyright © 2023 Hideki Kumagai et al.
                License:

                This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 9 November 2022
                Date revision received : 26 April 2023
                Date accepted : 13 June 2023
                Categories
                Subject: Case Report

                ScienceOpen disciplines: Surgery
                Data availability:
                ScienceOpen disciplines: Surgery

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