Laparoscopic resection of a solitary intrahepatic diverticular choledochal cyst in adult: a new clinical subtype?

Introduction

Choledochal cysts (CCs) are congenital or acquired cystic dilations of the intra- and/or extrahepatic bile ducts. This abnormal dilation can occur as a single cyst or multiple cysts. The incidence of CCs varies significantly between Western and Eastern populations with rates ranging from 1/100,000 to 1/150,000 and 1/1,000, respectively (1). In a multi-institutional analysis of 394 patients who underwent CC resection, 84.5% of the CC patients were symptomatic while 15.5% were asymptomatic (2). Common presentations include abdominal pain, jaundice, and a right upper quadrant mass. As an extremely rare type of CC, solitary diverticular intrahepatic choledochal cysts (SDICCs) are often misdiagnosed as simple hepatic cysts (SHCs) due to the similar radiographic features and high prevalence of SHC (3), which in turn affects the therapeutic outcomes and prognosis of patients (4). In this article, we present the case of a patient with SDICC, who was diagnosed and treated at Daping Hospital, and systematically summarize the clinical features of SDICC, along with its diagnostic and therapeutic approaches, based on our own experience and a literature review.

Case presentation

A 55-year-old woman was admitted to the Department of Hepatobiliary Surgery of Daping Hospital following the discovery of an intrahepatic cyst with stone formation via B-ultrasound. The patient had been diagnosed with SHC at another hospital some 20 years earlier, and had undergone puncture and drainage at that time. The fluid drained out of the cyst was bile, indicating that the cystic lesion was a CC. The patient did not undergo further treatment at that time because she was asymptomatic.

After admission to the Department of Hepatobiliary Surgery, no positive symptoms or physical signs were observed. An upper abdominal enhanced computed tomography (CT) scan revealed a cystic lesion 5.5 cm × 6.1 cm in size located in the left inner lobe and right anterior lobe of the liver, with a biliary stone inside (Figure 1A,1B). The cyst was closely adjacent to the gallbladder, and a septum between them was observed. Magnetic resonance cholangiopancreatography (MRCP) suggested that the cyst was close to the porta hepatis and adjacent to the gallbladder, but it was unclear whether it was connected to the bile duct (Figure 1C,1D). An initial diagnosis of a solitary intrahepatic choledochal cyst (SICC) or duplicated gallbladder was considered.

Figure 1 Preoperative CT and MRCP were performed. (A) Axial abdominal CT scan showing a solitary intrahepatic cyst located in the porta hepatis area. A biliary stone was clearly visible; (B) a coronal abdominal CT scan revealed that the cyst was closely adjacent to the gallbladder and that there was a septum between them; (C,D) MRCP revealed a close relationship between the cyst and the gallbladder, but it was unable to delineate the exact origin of the cyst along the biliary tree. CC, choledochal cyst; BS, biliary stone; GB, gallbladder; CD, cystic duct; CBD, common bile duct; LHD, left hepatic duct; CT, computed tomography; MRCP, magnetic resonance cholangiopancreatography.

To further clarify the relationship between the cyst and the bile duct, percutaneous transhepatic cystography (PTC) was performed on the patient. Following the injection of the contrast agent (150 mL iohexol 240), the cyst, common bile duct (CBD), left hepatic duct (LHD) and right hepatic duct (RHD), cystic duct, and gallbladder appeared one by one under X-ray fluoroscopy (Figure 2). It was confirmed that the cyst was not directly connected to the gallbladder, and other than the RHD, the cyst was not directly connected to any other intrahepatic bile ducts. The patient was diagnosed with a SDICC. After full discussion with a multidisciplinary team, and obtaining informed consent from the patient, laparoscopic resection of the SDICC and gallbladder was planned.

Figure 2 Preoperative PTC. Following the injection of the contrast agent, the cyst, bile ducts, and gallbladder emerged one by one. (A) The entire cyst and the common bile duct were clearly visible; (B) the intrahepatic bile ducts and cystic duct appeared; (C) part of the gallbladder can be seen; (D) this image revealed that the biliary cyst was not connected to the gallbladder, LHD, or common hepatic duct. Although the exact origin of the cyst cannot be determined, the above results strongly suggested a high probability of connection between the cyst and the RHD. CC, choledochal cyst; CBD, common bile duct; CD, cystic duct; LHD, left hepatic duct; RHD, right hepatic duct; GB, gallbladder; PTC, percutaneous transhepatic cystography.

During the laparoscopic exploration, a biliary cyst in the left inner and right anterior lobes was observed, which was almost completely intrahepatic, with a small portion exposed on the inferior surface of the liver just to the left of the gallbladder. There was a dense adhesion between the lower third of the gallbladder and the cyst. After careful dissection, the gallbladder was fully freed, and then resected. Electrocautery and a harmonic scalpel were then used to dissect the biliary cyst from the liver parenchyma along its wall. The outer surface of the cystic wall was smooth, and no intrahepatic bile ducts were observed to be connected to the biliary cyst. The right upper wall of the cyst was closely adjacent to the major branches of the middle hepatic vein (MHV), and the bottom wall adhered closely to the hilar bile duct. Dissection of the hilar bile duct revealed that the biliary cyst originated from the RHD. After an incision from the inferior wall of the cyst, a black mulberry-like stone with a diameter of approximately 1.5 cm was observed. The inner wall of the cyst was smooth, and no neoplasms were observed. Finally, the CC was completely resected, and the communication channel was sutured with 5-0 Prolene (Figure 3). The surgery went smoothly with 60 mL of blood loss and a 3.5-hour operative time, and the patient recovered well after surgery and was discharged on postoperative day 7.

Figure 3 Laparoscopic resection of the SDICC. (A) Laparoscopic exploration revealed that the biliary cyst was located near the porta hepatis, and was almost completely intrahepatic, with a small portion exposed on the inferior surface of the liver just to the left of the gallbladder. There was dense adhesion between the gallbladder and the cyst; (B) dissection of the biliary cyst along the wall. The right upper wall of the cyst was closely adjacent to the major branches of the MHV; (C) dissection of the LHD, which was closely adjacent to the left inferior wall of the cyst; (D) the orifice and the stone could be clearly observed after opening the biliary cyst; (E) after removing the biliary cyst, the stumps of the cystic duct, cystic artery and communication channel could be observed; (F) surgical specimens of the biliary cyst, gallbladder and stone. CC, choledochal cyst; GB, gallbladder; MHV, middle hepatic vein; LHD, left hepatic duct; BS, biliary stone; RHD, right hepatic duct; CD, cystic duct; CBD, common bile duct; SDICC, solitary diverticular intrahepatic choledochal cyst.

Postoperative pathology confirmed the diagnosis of a CC (Figure 4). The patient was followed up for 12 months without any complications or discomfort. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for publication of this article and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Figure 4 H&E staining of the specimens confirmed the diagnosis of SDICC. (A,B) H&E staining of the biliary cyst showed that the cyst was composed of fibrous cystic wall tissue, with no epithelial lining on the inner wall, and a thin layer of smooth muscle tissue was observed (A: 100×; B: 400×); (C,D) H&E staining of the gallbladder specimen, which was used as a control (C: 100×; D: 400×). H&E, hematoxylin and eosin; SDICC, solitary diverticular intrahepatic choledochal cyst.

Discussion

The exact etiology of CC remains unknown, and different theories have been put forward for the etiologies of different types of CCs. For example, Todani type I and IV CCs likely develop as a result of an anomalous pancreaticobiliary junction (APBJ), while Babbitt’s theory is the most popular theory for explaining the etiologies and pathophysiologies of CCs (5). The APBJ is a long common channel formed by the biliary and pancreatic ducts that is not covered by the sphincter, and allows for the backflow and mixing of pancreatic and biliary secretions, which not only increases the pressure in the bile duct but also activates pancreatic enzymes. These changes eventually cause dilation, inflammation, dysplasia, and malignancy of the biliary tree. Additionally, some theories postulate that CC may be purely congenital, arising from the abnormal duplication of either the biliary tract for Todani type II CCs, or the duodenum for type III CCs during embryonic development, or that CC may serve as a secondary manifestation of distal biliary dyskinesia (6,7). The etiology of Caroli disease, also known as Todani type V CC, is presumed to be related to a halt in the remodeling of the ductal plates (8).

As mentioned above, there are multiple CC classifications. In 1959, Alonso-Lej et al. (9) classified extrahepatic bile duct dilatation into three types based on cyst location. In 1977, Todani et al. (10) expanded the classification to include intrahepatic bile duct dilatations, resulting in a modified classification that includes five types of CCs, and is the most widely used by clinicians. However, Todani’s classification system was based on a small case series, and thus cannot fully reflect the complexity of CCs and cannot be used to accurately distinguish among the pathophysiological types of CCs. The treatment strategy and prognosis of CCs are not closely related to Todani’s classification.

Dong et al. (11) proposed a new classification system for CCs based on an analysis of 434 cases, which provides more explicit guidance for surgical decision making and the selection of therapeutic approaches for CCs. Dong’s classification system divides the biliary tree into the following three regions: peripheral intrahepatic bile ducts, central intrahepatic bile ducts (including the convergence of the LHD and RHD, and grade 1–2 branches), and extrahepatic bile ducts [the common hepatic duct (CHD) and CBD]. Based on the location of the cystic dilatation and the involvement of the biliary tree, CC can be classified into four types and eight subtypes (Figure 5); type A cysts represent approximately 6% of CCs and are characterized by cystic dilation of the peripheral intrahepatic bile ducts (Caroli’s disease); type B cysts represent 3% of CCs and involve cystic dilation of the central intrahepatic bile ducts; type C cysts represent 69% of CCs and are characterized by cystic dilation of the extrahepatic bile ducts; and type D cysts represent 22% of CCs and involve multiple dilations affecting both the intrahepatic and extrahepatic biliary tree (Figure 5B).

Figure 5 Schematic diagrams of the SDICC and Dong’s classification of CCs. (A) Schematic diagram of the SDICC reported in this study, which should be considered a new CC subtype; (B) Dong’s classification of CCs: type A: cystic dilations of the peripheral intrahepatic bile ducts (Caroli’s disease, subtype A1: cystic dilations of the bile ducts confined to lobes or segments; subtype A2: cystic dilations involving the entire intrahepatic biliary tree); type B: cystic dilations of the central intrahepatic bile ducts (subtype B1: solitary cystic dilation of the central hepatic ducts confined to the unilateral lobe; subtype B2: multiple cystic dilations involving the central hepatic ducts of the bilateral lobes); type C: cystic dilation of the extrahepatic bile ducts (subtype C1: cystic dilation involving the upper portion of common bile duct; subtype C2: cystic dilation involving the intrapancreatic portion of common bile duct); type D: multiple cystic dilations involving both the intrahepatic and extrahepatic biliary tree (subtype D1: multiple cystic dilations involving the central intrahepatic and extrahepatic bile ducts; subtype D2: multiple cystic dilations involving the peripheral intrahepatic and extrahepatic bile ducts). CC, choledochal cyst; SDICC, solitary diverticular intrahepatic choledochal cyst.

We performed a systematic literature search of the MEDLINE/PubMed, EMBASE, and Web of Science databases in April 2024 using the key words “choledochal cysts”, “solitary”, “intrahepatic”, and “diverticular”. All articles published in English and in peer-reviewed journals over the last 50 years were included in our study. We also checked the reference lists of each relevant study that resulted from this search to identify any other relevant articles. A total of seven articles containing nine patients with SICC were identified (12-17). Among the SICC patients, four patients had SDICC (Table 1), including 1 adult patient and 3 infants (15-17). All the SDICC patients underwent open surgery, of whom, one underwent hepatectomy and three underwent cystectomy. Despite the fact that only five cases of SDICC (including our case) have been reported, we summarize some of the clinical features of the SDICC cases as follows: (I) all five cases of SDICC occurred in the porta hepatis region; (II) there was a connection between the cyst and the CHD or RHD/LHD in all the reported SDICC cases; and (III) the cyst usually formed dense adhesions with the hilar bile ducts and the gallbladder.

SDICC has different anatomic characteristics, surgical approaches, and prognoses compared to those of non-diverticular SICC, which can be classified as Todani type V or Dong type B1. Because no peripheral bile ducts communicate with the cyst, and the cyst has only one connection to the central bile ducts, a SDICC can be fully mobilized and completely resected with no need for partial hepatectomy or cystojejunostomy. Saito et al. classified diverticular CCs involving the LHD or RHD as Todani type II (18), but those CCs are all located extrahepatically, and the cyst in our case was located intrahepatically. Therefore, it is our view that SDICC should be considered a new clinical type of CC that can be classified as a subtype of Todani type V, or Dong type B (Figure 5A). The establishment of a new CC subtype is expected to attract further attention from clinicians, and minimize the misdiagnosis of intrahepatic CCs. Importantly, the surgical treatment of this newly identified subtype is simple cystectomy, in contrast to that of other intrahepatic CCs, which often require hepatectomy or hepaticojejunostomy.

It is difficult to make a definitive diagnosis of SDICC before surgery. SDICC is prone to being misdiagnosed as SHC due to its similar radiographic features. Notably, MRCP, while useful for displaying the entire biliary tree, was unable to delineate the exact origin of the cyst along the bile ducts. Hepatobiliary iminodiacetic acid (HIDA) scan is another non-invasive imaging method that can be used to confirm biliary connection to a liver cyst; however, it is also limited in its ability to delineate anatomic details (19). Therefore, we strongly recommend PTC as the preferred diagnostic modality for SDICC. The advantages of PTC not only include its ability to ascertain the nature of the cyst fluid through puncture drainage but also its ability to elucidate the relationship between the cyst and bile ducts and even determine the precise origin of the cyst along the biliary tree via dynamic imaging of the cyst, intra-/extrahepatic bile ducts, and gallbladder. Certainly, intraoperative cholangiography or cystography is also valuable to clarify the anatomical relationship between the cyst and bile duct, particularly in cases in which dense inflammatory adhesions exist around the cyst and porta hepatis.

To our knowledge, this is the first reported case of laparoscopic SDICC resection. Compared with the traditional open surgery, laparoscopic cystectomy has the advantages of minimal trauma, less bleeding, and more precise dissection, which lead to the maximum preservation of normal liver tissue and hilar structure, thereby improving patient outcomes. The difficulty of the surgery relates to the dissection and determination of the confluence of the cyst with the central bile ducts. In most cases, it is very difficult to mobilize the ductal stalk of biliary cysts for suture ligation due to the dense adhesion between the cyst and the porta hepatis. Therefore, a cyst incision should be made, and the internal orifice of the cystic duct can usually be observed in the bottom wall of the cyst. The cystic wall was removed as much as possible while remaining above the orifice, thus avoiding the dissection of the confluence with the bile duct. After the circumferential transection of the cyst neck using either an electrocautery hook dissector or ultrasonic shears, the internal orifice should be sutured.

The major limitation of this study is that we only provided descriptive data for this patient. Due to the small sample size, we could not compare the benefits of laparoscopic cystectomy and open cystectomy/hepatectomy. The small sample size also impeded our ability to reach a firm consensus as to the significance of this new clinical subtype of CCs in relation to existing classifications. Dong’s classification system more accurately reflects the complexity of biliary dilations and is more closely related to treatment strategies than Todani’s classification system; however, it has not been widely accepted internationally and still requires further assessment. Further, neither Todani’s classification system nor Dong’s classification system involves the concept of pancreaticobiliary maljunction, which may significantly affect the choice of operative procedures. Thus, the current classification systems for CCs may need to be further refined in the future.

In conclusion, we reported an extremely rare case of SDICC that was highly prone to being misdiagnosed as SHC and was successfully resected via laparoscopy. According to our findings, preoperative PTC or intraoperative cholangiography are effective and necessary to elucidate the anatomical details of such cysts, which in turn will facilitate the selection of the optimal surgical approach. We contend that SDICC should be considered a novel subtype of CC due to its distinctive anatomical characteristics, surgical approaches, and prognosis. Clinicians should be highly alert and should consider the presence of SDICC in patients with isolated intrahepatic cystic lesions.

Acknowledgments

Funding: This work was funded by a key joint project of Chongqing Health Commission and Science and Technology Bureau (No. 2024ZDXM007 to G.C.), and a key medical research project of “Artificial Intelligence Plus” (No. ZXAIZD003 to G.C.).

Footnote

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1020/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for publication of this article and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Cazares J, Koga H, Yamataka A. Choledochal cyst. Pediatr Surg Int 2023;39:209. [Crossref] [PubMed]
2. Soares KC, Kim Y, Spolverato G, Maithel S, Bauer TW, Marques H, Sobral M, Knoblich M, Tran T, Aldrighetti L, Jabbour N, Poultsides GA, Gamblin TC, Pawlik TM. Presentation and Clinical Outcomes of Choledochal Cysts in Children and Adults: A Multi-institutional Analysis. JAMA Surg 2015;150:577-84. [Crossref] [PubMed]
3. Lopes Vendrami C, Thorson DL, Borhani AA, Mittal PK, Hammond NA, Escobar DJ, Gabriel H, Recht HS, Horowitz JM, Kelahan LC, Wood CG, Nikolaidis P, Venkatesh SK, Miller FH. Imaging of Biliary Tree Abnormalities. Radiographics 2024;44:e230174. [Crossref] [PubMed]
4. Sun Z, Liu B, Shu B, Huang X, Wang L, Yang S. Clinical characteristics of solitary intrahepatic biliary cyst. Biosci Trends 2023;17:409-12. [Crossref] [PubMed]
5. Babbitt DP. Congenital choledochal cysts: new etiological concept based on anomalous relationships of the common bile duct and pancreatic bulb. Ann Radiol (Paris) 1969;12:231-40. [PubMed]
6. Kusunoki M, Yamamura T, Takahashi T, Kantoh M, Ishikawa Y, Utsunomiya J. Choledochal cyst. Its possible autonomic involvement in the bile duct. Arch Surg 1987;122:997-1000. [Crossref] [PubMed]
7. Kagiyama S, Okazaki K, Yamamoto Y, Yamamoto Y. Anatomic variants of choledochocele and manometric measurements of pressure in the cele and the orifice zone. Am J Gastroenterol 1987;82:641-9. [PubMed]
8. Levy AD, Rohrmann CA Jr, Murakata LA, Lonergan GJ. Caroli's disease: radiologic spectrum with pathologic correlation. AJR Am J Roentgenol 2002;179:1053-7. [Crossref] [PubMed]
9. Alonso-Lej F, Rever WB Jr, Pessagno DJ. Congenital choledochal cyst, with a report of 2, and an analysis of 94, cases. Int Abstr Surg 1959;108:1-30. [PubMed]
10. Todani T, Watanabe Y, Narusue M, Tabuchi K, Okajima K. Congenital bile duct cysts: Classification, operative procedures, and review of thirty-seven cases including cancer arising from choledochal cyst. Am J Surg 1977;134:263-9. [Crossref] [PubMed]
11. Dong JH, Zeng JP, Feng XB. Clinical classification and surgical treatment of biliary dilatation: application and consideration. Chin J Dig Surg 2017;16:775-6.
12. Austin RM, Sussman S, McArdle CR, Kim D, Elboim C. Computed tomographic and ultrasound appearances of a solitary intrahepatic choledochal cyst. Clin Radiol 1986;37:149-50. [Crossref] [PubMed]
13. Carrascosa MF, Salcines-Caviedes JR, Rodríguez-Sanjuan JC, Cano-Hoz M, Gómez-Román J. A rare benign condition: intrahepatic giant biliary cyst in an adult. Dig Liver Dis 2014;46:384-5. [Crossref] [PubMed]
14. Chen W, Zhang T, Liu L. Congenital solitary intrahepatic biliary cyst. ANZ J Surg 2023;93:734-5. [Crossref] [PubMed]
15. Brown DK, Kimura K, Sato Y, Pringle KC, Abu-Yousef MM, Soper RT. Solitary intrahepatic biliary cyst: diagnostic and therapeutic strategy. J Pediatr Surg 1990;25:1248-9. [Crossref] [PubMed]
16. Burke ZD, Boechat I, Tabsh K, Deugarte DA. Solitary diverticular type V bile duct cyst. Pediatr Surg Int 2014;30:245-7. [Crossref] [PubMed]
17. Salles A, Kastenberg ZJ, Wall JK, Visser BC, Bruzoni M. Complete resection of a rare intrahepatic variant of a choledochal cyst. J Pediatr Surg 2013;48:652-4. [Crossref] [PubMed]
18. Saito T, Ando H, Ishihara S, Itoi T, Urushihara N, Otsuka M, Koshinaga T, Nagakawa Y, Hamada Y, Morotomi Y. Does Congenital Biliary Dilatation Todani Type II (Diverticular Type) Really Exist? J Pediatr Surg 2024;59:240-6. [PubMed]
19. Brown ZJ, Baghdadi A, Kamel I, Labiner HE, Hewitt DB, Pawlik TM. Diagnosis and management of choledochal cysts. HPB (Oxford) 2023;25:14-25. [Crossref] [PubMed]