Laparoscopic cholecystectomy in patients with portal cavernoma without portal vein decompression.

INTRODUCTION: Laparoscopic cholecystectomy (LC) in patients with extrahepatic portal vein obstruction causing portal cavernoma (PC) is considered high risk because of portosystemic collateral veins in the hepatocystic triangle. The literature is limited to isolated case reports. We describe our experience of LC in patients with PC. PATIENTS AND METHODS: Data of patients with PC who underwent LC for symptomatic gallstones or related complications was reviewed. Patients with simultaneous cholecystectomy with splenorenal shunt and open cholecystectomy were excluded. Pre-operative evaluation consisted of complete blood count, international normalisation ratio and liver function tests, ultrasound of the abdomen with Doppler, contrast-enhanced computerised tomography, magnetic resonance cholangiopancreatography and esophagogastroscopy as indicated. A standard four-port LC was performed. The technical principles followed were to avoid injury to the collateral veins, liberal use of energy sources and division of dominant collateral veins between clips.
RESULTS: Seven adult patients including three females underwent LC. Three patients had thrombosis of previous surgical shunt with persistent PC. The remaining four patients did not have any indication for shunt surgery. Successful LC was performed in six patients. The median duration of surgery was 170 (130-250 min). Blood transfusion was not required. All the patients had uneventful post-operative recovery. The histopathology of gall bladder consists of acute cholecystitis in three patients and chronic cholecystitis in four.
CONCLUSION: LC is feasible in patients with PC at a centre with experience in both laparoscopic and portal hypertension surgeries. Excellent outcome with low rate of conversion to open surgery can be achieved.

INTRODUCTION

Gallstone disease has high worldwide prevalence, management costs and the risk of development of gallstone symptoms and complications.[1] Gallstones are more than two times common in patients with portal hypertension compared to the control population. Gallstones are equally common in cirrhotic and non-cirrhotic portal hypertension.[2] Extrahepatic portal vein obstruction leading to portal cavernoma (PC) is a main cause of non-cirrhotic portal hypertension in India. Portal cavernoma cholangiopathy (PCC) is defined as abnormalities in the extrahepatic biliary system including the cystic duct and gall bladder (GB) with or without abnormalities in the first- and second-generation biliary ducts in a patient with PC.[3] Gallstones may contribute to the natural history of PCC from asymptomatic to symptomatic stage. Clinically, these patients present as biliary colic, cholecystitis or choledocholithiasis causing biliary obstruction or cholangitis.

Symptomatic gallstones and choledocholithiasis both warrant cholecystectomy, provided it is feasible and safe. Laparoscopic cholecystectomy (LC) is the standard for symptomatic GB stones including acute calculous cholecystitis.[4] The safety of LC in the presence of cirrhosis and portal hypertension is well established.[5] The presence of PC is considered a relative contraindication for LC because of the presence of large collateral venous channels in the hepatocystic triangle.[6] Few successful LCs in patients with PC have been reported.[78] We share a series detailing our experience of performing LC in patients with PC.

PATIENTS AND METHODS

This study is a retrospective review of prospectively maintained data at the Department of Hepato-Pancreato-Biliary Surgery at the Institute of Liver and Biliary Sciences, New Delhi. Patients with PC, who were attempted LC for symptomatic gallstone disease and related complications, were reviewed. Patients who underwent cholecystectomy with splenorenal shunt and upfront open cholecystectomy were excluded.

Demographic parameters including age and sex were recorded, along with a detailed clinical history regarding abdominal pain, history of jaundice, gastrointestinal bleeding, prior surgery for portal hypertension and endoscopic interventions. Laboratory evaluation included complete blood count, liver function tests and international normalisation ratio. The radiological evaluation consisted of an ultrasound of the abdomen with Doppler, contrast-enhanced computerised tomography (CECT) of the abdomen and magnetic resonance cholangiopancreatography (MRCP) as indicated. Upper gastrointestinal endoscopy was done as part of the routine evaluation of these patients. Blood was cross-matched and two units of packed cells were arranged. Continuous variables are described as median (range) and categorical variables as percentages. Post-operative course was monitored and hospital stay was recorded. Patients were regularly followed up.

Operative technique

Infraumbilical incision was placed and deepened. A 10-mm camera port was inserted by open technique and pneumoperitoneum was established. Subsequent ports were placed under vision for a standard 'four-port' LC. It included a 10-mm epigastric port, and additional two 5-mm ports were placed in the right midclavicular line and the right anterior axillary line. Adhesiolysis was performed [Figure 1a] when required. Energy devices were used liberally. Calot's triangle was carefully dissected to avoid bleeding [Figure 1b]. This was aided by ultrasonic shears (Harmonic Ace™, Ethicon Endo-Surgery, USA), sealer/divider (LigaSure™, Medtronic, Dublin, Ireland) and a 5-mm bipolar diathermy.

Figure 1

Steps of laparoscopic cholecystectomy in the presence of portal cavernoma. Arrows showing portosystemic collateral veins. (a) Large venous collaterals around the gall bladder and hepatoduodenal ligament. (b) Dissection of triangle of Calot. (c) Clipping of dominant collateral vein (d) clipping the cystic artery (e) clipping of cystic duct with a collateral vein together (f) dominant collateral vein during dissection of GB from the liver bed

Dominant collateral veins were preferentially divided between two clips or Hem-o-lok (Hem-o-lok clip, Weck Closure Systems, Research Triangle Park, NC) [Figure 1c]. The cystic artery was divided between 5 mm Hem-o-lok clips [Figure 1d]. The cystic duct along with the collaterals was divided between two 5/10 mm Hem-o-lok clips [Figure 1e]. Endostapler was used for wide cystic ducts. The GB is gently retracted to avoid bleeding from the collateral veins in the GB fossa [Figure 1f]. Dominant veins were again clipped and divided while dissecting the GB of the liver bed. GB was retrieved through the umbilical port. Haemostasis was achieved and an abdominal drain was placed if needed.

RESULTS

From 2010 to 2018, a total of 12 patients with PC due to extrahepatic portal vein obstruction underwent cholecystectomy. Four patients underwent cholecystectomy during proximal splenorenal shunt (PSRS). Open cholecystectomy was performed in one patient. Seven patients (three females) underwent LC are discussed here. The median age of these patients was 40 years (23–57 years). Three patients had prior PSRS about 7, 2 and 1 year ago. These patients had shunt thrombosis and persistent cavernoma. The demographic and pre-operative parameters of these patients are described in Table 1. Only one patient had a history of upper gastrointestinal bleeding and underwent PSRS for the same. One patient underwent endoscopic clearance of common bile duct stones before cholecystectomy. Three patients presented with acute cholecystitis. One patient underwent emergency LC and two patients had interval cholecystectomy.

Table 1

Clinical and laboratory details of the patients

Parameter	n/n (range)
Age (years)	40 (23-57)
Sex (male:female)	3:4
Previous surgical shunt	3
Endotherapy	3
Abdominal pain	5
History of jaundice	2
Variceal bleeding	1
Haemoglobin (g/dl)	11 (8.4-15)
Total leucocyte count (109/L)	7.2 (2.0-10.4)
Platelet count (109/L)	159 (102-464)
International normalisation ratio	0.98 (0.9-1.4)
Serum bilirubin (mg/dl)	0.85 (0.3-1.6)
Albumin (g/dl)	3.7 (3.1-4.5)

The important laboratory parameters are summarised in Table 1. The median operative time was 170 min (130–250 min). There was no blood transfusion required in any of these cases. The patients recovered well and were discharged within 2 days of surgery. The histopathology of GB consists of acute cholecystitis in three patients and chronic cholecystitis in the rest. Patients are asymptomatic at a median follow-up of 34 months (18–60 months).

DISCUSSION

Gallstones are seen in one-third and bile duct stones in 18% of symptomatic PCC patients.[9] In another study, gallstones and common bile duct stones were observed in 54% and 23% of symptomatic PCC patients, respectively, compared to 0% and 2.5%, respectively, in asymptomatic patients.[10] The literature on endotherapy in PCC patients is limited to isolated case reports about cholecystectomy after endoscopic clearance of choledocholithiasis.[61112] Indication and timing of cholecystectomy in the absence of shuntable veins is not clear.

Regarding the surgical treatment of gallstones in PCC, the present literature is limited.[13] Obviously, the patients who got relieved with shunt surgery alone may not need it. The biliary enteric anastomosis group will invariably have cholecystectomy as part of the procedure. Large series involving the surgical management of PCC do not mention whether cholecystectomy was performed during the shunt surgery for the subgroup of patients with gallstones.[914] In the series involving surgical management of PCC of 39 patients, about 13 patients had gallstones, but only one patient required cholecystectomy after shunt surgery.[9] Around one-third of patients continue to have cholangiographic abnormalities and may suffer from repeat biliary symptoms.[15] Dokmak et al. reported the safety of supramesocolic surgery in the presence of PC. This series reported twenty cholecystectomies, and five out of them were performed only for gallstone-related indications. Three-port cholecystectomy were performed laparoscopically,[16] though the aetiology for PC in this series was predominantly secondary to pancreatitis.

In our series, we dealt with a subgroup of patients who were symptomatic for their gallstone disease. These patients did not have any of the indications to undergo PSRS. They did not have a history of ongoing upper gastrointestinal bleed, and if they had portal biliopathy, it was non-obstructive. Indications for cholecystectomy in our series were acute cholecystitis in three patients, recurrent biliary colic in three patients and choledocholithiasis in one patient. The patient with choledocholithiasis underwent prior endoscopic clearance. Acute cholecystitis and PC is a difficult scenario. Acute inflammation adds to the surgical difficulty. Medical management or radiological interventions have their limitations. Medical management alone will not be curative. Radiological interventions such as percutaneous cholecystostomy may not be feasible given the risk of injury to the collateral veins and higher risk of bleeding. Subsequent surgery after cholecystostomy may be more difficult.

Radiological evaluation in this setting is valuable. CECT and MRCP both were useful and complementary. Ultrasound with color Doppler is the first radiological investigation which readily detect gallstones and PC [Figure 2a]. The presence of portosystemic collaterals, their relationship to Calot's triangle, GB fossa and port sites, the presence of spontaneous portosystemic shunts, the status of previous surgical shunt, splenomegaly and the presence of free fluid are important aspects before planning for LC in these patients [Figure 2b]. MRCP provides details of biliary anatomy, presence and stage of portal biliopathy and stones in CBD [Figure 2c]. Three patients had undergone PSRS two in our centre and one patient in another centre. On CECT evaluation, the surgical shunts were thrombosed.

Figure 2

Pre-operative radiological evaluation: (a) Ultrasound with colour Doppler showing portal cavernoma. (b) Contrast-enhanced computerised tomography venous phase showing portal cavernoma (black arrow) and features of acute cholecystitis. (c) Magnetic resonance cholangiopancreatography showing features of thick-walled gall bladder with impacted large stone (white arrow) with mild dilatation of central intrahepatic biliary radicals

Laparoscopic approach is to be taken with caution. Every step in the procedure is important and the presence of portal hypertension and portosystemic collaterals to be kept in mind throughout the procedure. In our series, all the procedures were performed by surgeons experienced in minimal invasive techniques and portal hypertension surgery. Pre-operative CECT can guide about the location and size of collaterals, especially around the umbilicus. Paraumbilical collaterals to be avoided in first port placement, the falciform ligament and re-canalized umbilical vein in the border of the falciform are potential sites of bleeding during subsequent port placement. The two small ports can be placed by avoiding the site of collaterals at both the entry and exit points. We performed upfront open cholecystectomy in view of sizable collaterals at the port site. We encountered pericholecystic adhesions in most of the patients. Adhesions to the scar of previous surgery add to the difficulty.

Gentle handling of the GB and avoiding undue traction is rewarding. Liberal use of energy sources and immediate control of any venous ooze should be done before proceeding to the next step. Blunt dissection in the triangle of Calot is discouraged. In all the procedures, we encountered prominent collateral veins running close to the cystic duct. The cystic duct to be clipped with the collateral vein and attempt to dissect between the two structures may cause bleeding. We converted only one procedure to open surgery because of frozen Calot's triangle. No procedure was converted for intraoperative bleeding. Abdominal drain was kept in one case and was removed after 2 days.

This series shows the feasibility of such a procedure at a tertiary care centre with experience in both laparoscopic and portal hypertension surgeries. The indication for LC needs to be clear. We have narrated the algorithm we followed in the selection of patients with PC for LC [Figure 3]. With expertise, excellent outcomes with a low rate of conversion to open surgery can be achieved. This is the largest series ever reported for LC in the presence of PC [Table 2]. Principles to be followed for safe LC in patients with PC include meticulous dissection, to keep the dissection of triangle of Calot away from the hepatoduodenal ligament, achieve the critical view of safety, careful dissection of the GB from GB fossa, division of collaterals between clips and careful haemostasis.

Figure 3

Algorithm for cholecystectomy on the background of portal cavernoma

Table 2

Cholecystectomy with portal cavernoma previous experience

Author	Number	Previous PSRS	Laparoscopy/open
Bhatia P et al.[9]	2	No	LC
Dalvi AN et al.[10]	1	No	LC
Dokmak S et al.[13]	3	No	LC
Present series	7	No (4) Thrombosis (3)	LC (6) LC converted to open (1)

PSRS: Proximal splenorenal shunt, LC: Laparoscopic cholecystectomy

CONCLUSION

LC can be performed safely in patients with PC without decompression of portal vein or if the previous surgical shunt is thrombosed. The advantages of laparoscopy techniques can be extended to this subgroup of patients in whom the clinical management is challenging.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.