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Malignant Pancreatic Serous Cystic Neoplasms: Systematic Review With

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Malignant Pancreatic Serous Cystic Neoplasms: Systematic Review With Huh et al. BMC Gastroenterology (2016) 16:97 DOI 10.1186/s12876-016-0518-0 RESEARCH ARTICLE Open Access Malignant pancreatic serous cystic neoplasms: systematic review with a new case Jimi Huh1,2, Jae Ho Byun1*, Seung-Mo Hong3, Kyung Won Kim1, Jin Hee Kim1, Seung Soo Lee1, Hyoung Jung Kim1 and Moon-Gyu Lee1 Abstract Background: This study analyzes the clinicopathologic and radiologic characteristics of malignant serous cystic neoplasm (SCN) of the pancreas through systematic review and an institutional case report. Methods: A comprehensive literature search was performed in the MEDLINE database to identify studies on malignant SCNs of the pancreas that had detailed clinicopathologic and radiologic information. A computerized systematic search of our institutional database was also performed to identify cases of malignant SCN for addition to the systematic review. Using the final included cases, we analyzed the clinicopathologic and radiologic features of malignant SCNs of the pancreas. Results: A review of 136 candidate articles identified 26 studies with 26 cases that had detailed clinical information. Our institutional data search added one case. The systematic review of the 27 cases revealed that primary tumors (mean diameter 10.2 ± 4.0 cm) mainly involved the body and tail of the pancreas (n = 16) and frequently invaded adjacent organs (n = 19). Distant metastases occurred in 14 patients (synchronous, n = 5; metachronous, n = 8; both, n = 1), most commonly in the liver (n = 13). Imaging features of malignant SCNs of the pancreas were identical to the benign counterpart, except local invasion or distant metastases. The prognosis was excellent in that 17 were alive at the time of writing with a median follow-up period of 2 years. Conclusions: The malignant potential of SCNs of the pancreas should be considered in the diagnosis and management of patients with pancreatic SCNs. Keywords: Serous cystadenocarcinoma, Serous cystic neoplasms, Pancreas, Computed tomography, Magnetic resonance imaging Abbreviations: CT, Computed tomography; DP, Distal pancreatectomy; FDG, 18F-fludeoxyglucose; MR, Magnetic resonance; PAS, Periodic acid-schiff; PD, Pancreaticoduodenectomy; PET, Positron emission tomography; PPPD, Pylorus preserving pancreaticoduodenectomy; SCN, Serous cystic neoplasm; SI, Signal intensity; TP, Total pancreatectomy; WHO, World Health Organization * Correspondence: [email protected] 1Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, 88 Olympic-Ro 43-Gil, Songpa-Gu, Seoul 05505, Korea Full list of author information is available at the end of the article © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Huh et al. BMC Gastroenterology (2016) 16:97 Page 2 of 10 Background following search terms were used: (pancreas OR pancre- Serous cystic neoplasms (SCNs) of the pancreas are usu- atic) AND (“serous cystadenocarcinoma” OR “serous ally cystic epithelial neoplasms composed of cuboidal, cystic neoplasm”). Our search did not set any restriction glycogen-rich, epithelial cells that produce serous fluid [1]. or filter. To expand the search, the bibliographies of arti- Pancreatic SCNs represent approximately 10–16 % of cles that remained after the selection process were all kinds of cystic pancreatic lesions [2–5]. Since screened for other potentially suitable articles. Compagno et al. classified cystic neoplasms of the pan- creas into serous and mucinous types in 1978 [6], SCNs Institutional data search and case presentation were considered as a benign disease entity without risk Our institutional review board approved the search of of malignant transformation. This concept changed after electronic medical records for this study. We performed George et al. reported the first case of a malignant SCN a systematic computerized search of our institutional of the pancreas in 1989 [7]. Thereafter, the number of database (ABLE, Asan Medical Center) from January case reports or series of malignant SCNs of the pancreas 1996 to April 2015 using the diagnostic codes of ‘serous increased [4, 8–31]. Thus, SCNs of the pancreas are not cystic neoplasm of the pancreas’, ‘serous cystadenoma of considered totally benign, but have an extremely low the pancreas’,and‘serous cystadenocarcinoma of the malignant potential. Regarding the incidence of malig- pancreas’. Using these search terms, we identified 447 nant SCNs, the majority of literature reported less than patients initially diagnosed with SCN of the pancreas. 1 %, including the largest series which showed three ser- Among the 447 patients, only one case was confirmed as ous cystadenocarcinomas from 2622 patients [32], even serous cystadenocarcinoma of the pancreas. We ob- though a few literature reported 1–5 % [5, 18, 33]. Due tained an informed consent from the patient. We to its very rare chance to be malignant, the vast majority present the clinical course, pathologic findings, and im- of SCNs are safely observed without resection [34]. aging features of this case. We also included this case in As a result of their extreme rarity, the characteristics the systematic review of malignant SCNs. of malignant SCNs of the pancreas were not well ex- plored until the World Health Organization (WHO) Analysis of clinicopathologic and radiologic features classification published in 2010 established the definition For the malignant SCNs from the literature search and of serous cystadenocarcinoma and described its charac- our institution, we analyzed their clinicopathologic fea- teristics [1]. In the 2010 WHO classification, malignancy tures, patterns of metastasis and local invasion, treat- is defined by the presence of distant metastases regard- ment, and outcome. When imaging features of the less of benign-looking histologic features. However, the primary tumors and/or metastatic tumors were available, WHO classification is still under debate as many studies we also analyzed these imaging findings. have classified SCNs that invade surrounding organs as malignant SCNs even though there is no distant metas- Results tasis [4, 9, 12, 13, 16, 21, 22, 24, 25, 27, 29, 33]. There- Literature selection fore, in this article, we use the broad term ‘malignant Our study selection process is shown in Fig. 1. The lit- SCNs’ to include either SCNs with distant metastasis or erature search in the MEDLINE database generated 136 local invasion. initial candidate articles. After reviewing the titles and Despite the increasing number of cases of malignant the abstracts and excluding 22 review articles, two con- SCNs, there has been no systematic review to summarize ference abstracts, and 80 articles that were not in the the variable presentations of malignant SCNs and to field of interest for this study, 32 articles were initially provideaperspectiveofthisrarediseaseentity. selected for eligibility. The full text of the 32 articles was Therefore, we performed a systematic review of the retrieved. The search of the bibliographies of these arti- malignant SCNs of the pancreas with the addition of cles found four additional eligible studies. Among these our single case. 36 eligible studies with 42 cases, we further excluded three articles that were not in the field of interest and Methods seven studies that did not have detailed information on Systematic literature search pancreatic serous cystadenocarcinomas, and selected 26 A computerized search of the MEDLINE database was studies with 26 cases [4, 7–31]. We also included the conducted to find relevant studies published prior to present case from our institution; thus finally 27 cases April 30, 2015. Studies were eligible for inclusion if they were reviewed in this systematic review. described the clinicopathologic features, imaging find- ings, treatment, and outcome of the cases with regard to Presentation of our case malignant SCNs of the pancreas. Any type of publication A 52-year-old woman presented to our institution with a including case reports or case series was eligible. The palpable abdominal mass. On physical examination, a Huh et al. BMC Gastroenterology (2016) 16:97 Page 3 of 10 Fig. 1 Flow diagram for literature selection large, soft mass was palpable in the epigastrium. Results marker, and CD10. The epithelial cells of the tumor had of laboratory examinations and tumor markers (carci- cytoplasmic periodic acid-Schiff (PAS)-positive granules. noembryonic antigen and carbohydrate antigen 19–9) The histopathological diagnosis was serous cystadenoma were within the normal range. Serum chromogranin A of the pancreas. was 108 ng/mL, which was around the upper normal Five years later, the patient presented with abdominal limit (27–94 ng/mL). Contrast-enhanced computed tom- discomfort. On contrast-enhanced CT, there were mul- ography (CT) scans showed a 9 × 8 cm solid and cystic tiple liver masses/nodules that showed peripheral rim mass in the head of the pancreas (Fig. 2a). The per- enhancement (Fig. 2e). Under suspicion of liver metasta-
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