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

Kumagai, Hideki; Umemura, Akira; Nitta, Hiroyuki; Katagiri, Hirokatsu; Nishiya, Masao; Uesugi, Noriyuki; Sugai, Tamotsu; Sasaki, Akira

doi:https://doi.org/10.1155/2023/5825045

Case Reports in Surgery

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Abstract Introduction Case Presentation Discussion Conclusions Data Availability Consent Conflicts of Interest References Copyright Related Articles

Case Report | Open Access

Volume 2023 | Article ID 5825045 | https://doi.org/10.1155/2023/5825045

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

Hideki Kumagai,¹Akira Umemura,¹Hiroyuki Nitta,¹Hirokatsu Katagiri,¹Masao Nishiya,²Noriyuki Uesugi,²Tamotsu Sugai,²and Akira Sasaki¹

Academic Editor: Wei-bo Chen

Received09 Nov 2022

Revised26 Apr 2023

Accepted13 Jun 2023

Published24 Jun 2023

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.

1. Introduction

Intracholecystic papillary neoplasm (ICPN) is a relatively new concept established by the 2010 World Health Organization (WHO) classification [1]. According to this classification, ICPN is recognized as a counterpart of intraductal papillary mucinous neoplasm in the pancreas and intraductal papillary neoplasm of the bile duct [1]. Tumors are considered premalignant lesions [2, 3].

ICPN is rare, accounting for 0.4–1.5% of cholecystectomies and 6.4% of gallbladder cancers [1–3]. Therefore, there are limited previous studies on the diagnosis or surgical management of ICPN, and the prognosis of ICPN remains controversial.

Here, we report a rare case of extensively invasive gallbladder cancer arising in ICPN treated with pylorus-preserving pancreaticoduodenectomy (PPPD) and extended cholecystectomy and review the previous literature.

2. Case Presentation

A 75-year-old man presented to the hospital with jaundice that had been present for 1 month. He had a medical history of hypertension and non-tuberculosis mycobacterial infection but no surgical history. Laboratory findings showed elevated levels of serum bilirubin and liver enzymes: total bilirubin, 10.6 mg/dL; aspartate aminotransferase, 68 IU/L; alanine aminotransferase, 119 IU/L; and gamma-glutamyl transpeptidase, 393 IU/L. Serum carbohydrate antigen 19-9 was also elevated (54.8 U/mL), though carcinoembryonic antigen was within the normal range. Enhanced computed tomography (CT) revealed a well-enhanced tumor in the distal bile duct and dilation of the hepatic bile duct (Figure 1(a)). In addition, the gallbladder mucosa was thickened, with a homogeneous contrast effect (Figure 1(b)). Magnetic resonance imaging (MRI) showed a low T2 signal tumor in the common bile duct (Figure 2(a)), and magnetic resonance cholangiopancreatography (MRCP) showed dilation of the hepatic-sided bile duct from the tumor (Figure 2(b)). The thickened gallbladder walls had a homogeneous low T2 signal; however, liver invasion by the tumor was not significant. Endoscopic retrograde cholangiopancreatography (ERCP) revealed a filling defect in the distal bile duct, and the cystic duct was invisible (Figure 3(a)). Moreover, intraductal ultrasonography (IDUS) showed a papillary tumor in the common bile duct and indicated invasion of the bile duct subserosa (Figures 3(b) and 3(c)). Subsequent bile duct brushing cytology on ERCP and IDUS revealed adenocarcinoma, and the patient was diagnosed with distal bile duct cancer associated with adenomyomatosis of the gallbladder.

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The patient was referred to our hospital for surgical treatment, and we planned to perform PPPD for distal bile duct cancer with curative intent. Intraoperative findings revealed a thickened and indurated gallbladder wall, suggesting the coexistence of gallbladder cancer; thus, we performed PPPD and extended cholecystectomy. Intraoperative frozen-section analysis of the cut end of the hepatic bile duct was negative for the tumor. A macroscopic examination of the resected specimen revealed a papillary tumor that had extensively invaded the liver, cystic duct, bile duct, and pancreas (Figures 4(a) and 4(b)). Permanent histopathological findings indicated that the tumor was papillotubulary and had broad-based growth of columnar cells with mucus production in the gallbladder (Figures 5(a) and 5(b)). In addition, metastasis to the lymph nodes of the hepatoduodenal ligament was observed. Immunohistochemical analysis revealed that the tumor cells were positive for mucin (MUC)1, MUC5AC, and MUC6, but negative for MUC2 and p53 (Figures 5(c), 5(d), and 5(e)). Finally, the diagnosis of gastric-type ICPN was established according to the 2010 WHO classification. The postoperative course was uneventful, and the patient started adjuvant chemotherapy (tegafur/gimeracil/oteracil) 1 month after surgery. At the follow-up after 1 year, the patient had no recurrence.

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3. Discussion

We report the case of a patient with extensively invasive gallbladder cancer originating in ICPN treated with PPPD and extended cholecystectomy. Adsay et al. reported that invasiveness was observed in 55% of ICPN cases [1]; however, most patients with ICPN are found at an early stage incidentally by imaging studies, as mentioned below, and reports on advanced cases are limited [4–7]. We searched for previous reports on ICPN in PubMed using the keywords “intracholecystic papillary neoplasm” or “intracystic papillary neoplasm” and reviewed 39 cases [4–39], including the present case diagnosed as ICPN histopathologically (Table 1). The mean age of patients with ICPN was 66.3 years, and female patients outnumbered male patients, as previously reported [3]. Approximately half of the ICPNs have invasive components, as found by Adsay et al., however, our patient was the only patient with lymph node metastasis in our review.

Moreover, Adsay et al. reported that approximately half of the ICPNs develop in the right upper abdominal region, and the other half are incidentally found by imaging studies [1], which is similar to our findings summarized in Table 1. Conversely, jaundice is an uncommon symptom in ICPN, and there are few previous reports in the literature [4, 5, 25, 27]. Of the four patients, two patients suffered from jaundice resulting from a protruding tumor from the gallbladder to the common bile duct [4, 5]. Interestingly, the other two developed jaundice due to mucus production from the tumor [25, 27]. In the present case, histopathological findings revealed that the tumor had extensively invaded the bile duct; thus, the patient had obstructive jaundice owing to tumor invasion of the common bile duct rather than a protruding tumor from the gallbladder. Protruding or advanced tumors associated with ICPN can cause obstructive jaundice; moreover, mucus production from ICPN can lead to jaundice.

Distinguishing between ICPN and other gallbladder tumors using imaging studies is difficult. In our review, only 15.8% of patients with ICPN were diagnosed accurately before surgery. According to previous reports, ICPN is well-defined on enhanced CT and presents high or low T2 signal intensity and high diffusion-weighted imaging signal intensity on MRI [4, 7]. Fluorodeoxyglucose (FDG) accumulation in ICPN has been observed on FDG-positron emission tomography [5, 28]. However, these are non-specific findings that can be observed in other gallbladder tumors. Moreover, histopathological examinations, including cytology and biopsy are not diagnostic in terms of distinguishing between ICPN and other types of gallbladder carcinomas [4–7]. However, endoscopic ultrasound (EUS), including IDUS or peroral cholangioscopy (POCS) has shown the presence of a papillary tumor in most patients diagnosed with ICPN preoperatively [4–6, 25, 27]. EUS and POCS may provide a better definition of ICPN compared with other imaging modalities. In the present case, IDUS revealed a papillary tumor in the common bile duct. Therefore, clinicians should be familiar with ICPN, and make an effort to accurately diagnose it using multiple imaging techniques.

The treatment for ICPN is oncological resection; however, the selection of the optimal surgical procedure is often challenging. Simple cholecystectomy is sufficient for ICPN limited to the gallbladder mucosa without invasion. However, approximately half of the ICPN cases have an invasive component [1]. Moreover, some patients have ICPNs suspected of common bile duct invasion due to a protruding tumor from the gallbladder to the common bile duct [4, 5]. In the present case, CT, MRI, and ERCP findings indicated that the tumor was located in the distal bile duct, and IDUS suggested that the tumor had invaded the subserosa of the bile duct; therefore, we decided to perform PPPD. Moreover, intraoperative findings showed a thickened and indurated gallbladder wall, suggesting advanced gallbladder carcinoma; thus, we performed an extended cholecystectomy in addition to PPPD. Intraoperative frozen-section analysis of the cut end of the hepatic-sided bile duct confirmed no evidence of a tumor. To select the optimal surgical procedure, a comprehensive evaluation that considers preoperative imaging studies and intraoperative findings is essential. Notably, EUS, including IDUS, can be a useful tool for assessing tumor extension of ICPN.

Some studies have reported that ICPN with or without invasive carcinoma has a good prognosis, in contrast to other types of gallbladder carcinoma [1, 40, 41]. Adsay et al. reported that the 1-, 3-, and 5-year overall survival rates of non-invasive ICPN were 90%, 90%, and 78%, respectively [1]. In addition, the percentages of invasive ICPN were 69%, 60%, and 60%, respectively [1]. These overall survival rates are much better than those of other types of gallbladder carcinomas, which have an 18–30% 5-year survival rate [1, 42]. In contrast, a recent study reported that in a stage-matching analysis of gallbladder carcinoma, there was no difference between the prognosis of invasive carcinoma and other types of gallbladder carcinoma [43]. In our review, most ICPN patients had a good prognosis. We speculate that this was due to most ICPNs being resected at an early stage. However, our patient had advanced cancer originating from an ICPN with lymph node metastasis. Therefore, our patient was closely followed up with adjuvant chemotherapy.

The optimal choice of surgical procedure, including extended cholecystectomy, bile duct resection, and pancreaticoduodenectomy is essential for achieving complete oncological resection of the tumor. In addition, close postoperative follow-up is crucial for patients with ICPN, especially those with advanced cancer arising from the tumor, in accordance with other types of gallbladder carcinoma.

4. Conclusions

Accurate preoperative diagnosis of ICPN, including the extent of tumor invasion, is challenging; however, both EUS and POCS are effective tools for resolving these challenges. ICPN has been recognized as a tumor with a better prognosis compared with other types of gallbladder carcinoma; however, a recent study reported that the prognosis of these tumors is equivalent. The optimal choice of surgical procedure and close postoperative follow-up are essential for patients with ICPN, especially those with advanced cancer arising from the tumor.

Data Availability

Data supporting this research article are available from the corresponding author or first author upon reasonable request.

Written informed consent was obtained from the patient for publication of the case details.

Conflicts of Interest

The author(s) declare(s) that they have no conflicts of interest.

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Copyright © 2023 Hideki Kumagai et al. 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.

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