Introduction

Roux-en-Y hepaticojejunostomy1 – 4 is a standard approach for biliary reconstruction after bile duct resection, bile duct injury and liver transplantation, or to manage biliary obstruction. The incidence of complications following hepaticojejunostomy varies according to the indication, level of reconstruction and presence of associated vascular injury, and is influenced by a range of patient factors including sepsis, malignancy and malnutrition. Bile leak and stricture formation are the major sources of morbidity following hepaticojejunostomy. In most cases, these biliary complications can be managed with the use of minimally invasive techniques. However, in the acute setting, surgical intervention may be required to address severe sepsis and restore biliary drainage where minimally invasive techniques have failed or are not feasible. Reconstruction in this setting is challenging and options are limited. In this paper, we describe how we perform a portoenterostomy (or modified Kasai procedure5) in adults as a salvage procedure for major biliary complications following hepaticojejunostomy. We also present long-term results of the three patients who underwent this procedure over a 14-year period and review the current literature.

Surgical Technique

Preoperative Preparation

This procedure is usually undertaken as an emergency for the salvage of a few patients with intraabdominal sepsis following dehiscence of a hepaticojejunostomy performed previously. Portoenterostomy is not recommended as a routine approach but should be reserved for those patients in whom a mucosa-to-mucosa reanastomosis of the bile ducts to the bowel is considered either hazardous or not feasible. Hence, there are few specific preoperative investigations to be performed. Patients usually have cross-sectional imaging (computed tomography) that demonstrates free fluid and gas locules in the abdomen, especially in the subhepatic space (Fig. 1). Intrahepatic duct dilatation is usually not seen unless the ducts were dilated prior to the hepaticojejunostomy. Cross-sectional imaging may also demonstrate vascular injuries and portal vein thrombosis. Percutaneous transhepatic drainage may be considered if there is intrahepatic duct dilatation, and time and the patient’s condition permit. In addition, some patients may require insertion of percutaneous radiological drains to treat intraabdominal fluid collections prior to surgical intervention. However, usually, the patient needs a surgical exploration after adequate resuscitation, preferably in a critical care area. Broad spectrum antibiotics should be started and thromboprophylaxis continued.

Fig. 1
figure 1

Postoperative abdominal CT scan showing a large subhepatic fluid collection with gas locules, suggestive of an anastomotic dehiscence. The low attenuation areas in the right lobe of the liver suggest ischemia after an arterial injury

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Operative Procedure

We perform a laparotomy through the previous incision (usually a roof top) and extend it as necessary. The bile and intestinal contents are suctioned and samples are sent for microbial culture. The abdominal contents are inspected carefully and when the dehiscence is found at the hepaticojejunostomy (Fig. 2a), the anastomosis is taken down and the end of the Roux loop bearing the dehisced anastomosis is resected with a transverse linear cutting stapler (Fig. 2b). If the anastomosis is not at the end of the Roux loop (as in the case of a pancreaticojejunostomy being fashioned proximal to the hepaticojejunostomy), the edges of the jejunal anastomosis are freshened and the enterotomy enlarged appropriately. The bile duct remnant is then inspected. The ischemic segments of the ducts are excised (Fig. 2b) and the viable stumps inspected to determine if refashioning of the bilioenteric anastomosis is feasible. If possible, the hilar plate is lowered to determine if adequate length of viable duct may be obtained. In all three cases described, there was ischemia of the common hepatic duct (or right hepatic duct) extending to the hilum of the liver, thereby precluding safe bilioenteric anastomoses in these critically ill patients. The Roux loop of the jejunum is then incised longitudinally, long enough to accommodate the hepatic hilum (Fig. 2c). The posterior wall of the incised jejunum is then anastomosed to the posterior hepatic hilum with 3-0 or 4-0 interrupted polydioxanone (PDS® II, Ethicon, Edinburgh, UK) sutures (Fig. 2c). Care is taken to avoid the right and left hepatic arteries and the right and left branches of the portal vein. The sutures are preplaced and are tied once all the posterior wall sutures are in situ (Fig. 2d). One or two 4 F or 5 F feeding tubes are then inserted into the abdominal cavity and into the Roux loop of the jejunum separately at the antimesenteric border and then exteriorized via the longitudinal incision made in the Roux loop. These tubes are then inserted into the right and left hepatic ducts (or common hepatic duct) to serve as transanastomotic stents (Fig. 2d). The anterior layer of the anastomosis is then completed with 3-0 or 4-0 interrupted PDS (Fig. 2e). Once again, these sutures are preplaced and are tied once all the anterior wall sutures are in situ. If a hepatectomy has been performed previously, as in our second patient, the anastomosis is fashioned in a similar way between the Roux loop and the hepatic parenchyma surrounding the bile duct remnant. As the sutures traverse the hepatic capsule and parenchyma, care must be taken to apply adequate tension to the knots so that they are snug, but do not cheeswire through the hepatic parenchyma. Purse string sutures with 4-0 PDS are taken through the Roux loop to anchor the feeding tubes at the entry sites. A thorough peritoneal lavage is performed with 0.9% saline and we place a white swab at the site of the anastomosis to check for bile leaks. If bile leaks are detected, extra sutures may be necessary to seal the portoenterostomy. One or two tube drains are placed in the subhepatic space before closing the abdomen in layers.

Fig. 2
figure 2

Diagrammatic representation of a portoenterostomy being performed

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Postoperative Management

The early postoperative care is best managed in a critical care area as these patients have sepsis and multiorgan dysfunction. Antibiotics should be continued and changed if the intraoperative fluid or blood cultures dictate so. Patients may need ventilatory, nutritional (enteral or parenteral) and cardiovascular support in the form of inotropes. We leave the transanastomotic stents in situ for 2 to 3 weeks after portoenterostomy subsequent to which we perform a contrast study to confirm patency of the anastomosis and exclude an ongoing bile leak. The stents are removed if these conditions are fulfilled and the abdominal drains are removed 2 to 3 days later if no bile drains through them. Patients are discharged from hospital once they fulfil the discharge criteria (i.e. self-caring, mobile, on oral nutrition and not requiring intravenous analgesia).

Long-Term Management

Liver function tests are monitored at two-monthly intervals and episodes of cholangitis are treated promptly with appropriate antibiotics. Derangement of liver function tests accompanied with prutitus may indicate an anastomotic stricture and necessitate cross-sectional imaging (magnetic resonance cholangiopancreatography or computed tomography). The presence of an anastomotic stricture requires percutaneous transhepatic cholangiography and balloon dilatation. A refractory dominant stricture may require a subsequent hemihepatectomy and redo hepaticojejunostomy to either the right or left hepatic duct, but this has not been necessary so far in our practice.

Patient Series and Results

Patient 1

A 34-year-old man who had undergone a split liver transplant from a heart-beating donor 2 years previously for primary sclerosing cholangitis, presented in extremis with peritonitis and severe sepsis. He had had an unremarkable post-transplantation history. At laparotomy, the jejunal limb of the retrocolic hepaticojejunostomy was found to be ischemic because of an internal volvulus. A damage control laparotomy was performed: the hepaticojejunostomy was taken down, the Roux limb excised and a 6 F feeding tube was inserted into the common hepatic duct with a tube drain left in the subhepatic space. Two days later, the patient underwent surgical reexploration. As the hepatic duct had been divided close to the level of the hilar plate, a hepaticojejunostomy was not feasible. Reconstruction was, therefore, undertaken using a retrocolic Roux-en-Y portoenterostomy with interrupted 3-0 PDS, with a 4 F feeding tube used as a transjejunal transanastomotic stent. External peritoneal drainage was effected via two tube drains. He remained on the ICU/HDU for 3 weeks and was discharged from hospital 37 days after his original presentation. Over the 14 years following this emergency presentation, he has had several episodes of self-limiting cholangitis, but no evidence of anastomotic stricturing. The serum bilirubin 14 years later was normal (11 μmol/l) with a borderline elevation of alkaline phosphatase (233 U/l).

Patient 2

A 68-year-old man underwent an extended left hemihepatectomy for a Bismuth type 3b cholangiocarcinoma (pT1, N0, Pn1, R0). Biliary reconstruction was undertaken with a retrocolic hepaticojejunostomy with a right hepatic duct-to-mucosa anastomosis using an interrupted 5-0 PDS across a 4 F stent with external peritoneal drainage via a tube drain. On the third postoperative day, he developed severe sepsis necessitating mechanical ventilation and escalating inotropic support. Bile was present in the abdominal drain. At surgical reexploration, the right hepatic duct stump was found to be ischemic with an associated dehiscence of the hepaticojejunostomy. The non-viable right hepatic duct was resected, exposing the anterior and posterior divisions. Reconstruction was achieved with a Roux-en-Y portoenterostomy on a single jejunal limb, using interrupted 4-0 PDS. Two 4 F feeding tubes were used as transjejunal transanastomotic stents, one in each division of the right hepatic duct. Two tube drains were placed in the subhepatic space and the patient transferred to the ICU where he remained for several weeks. The transanastomotic stents were removed after 30 days after confirmation of patency and absence of an anastomotic leak. The abdominal drains were removed 33 days after reoperation and the patient was eventually discharged from hospital 78 days after the original procedure. He remained well and disease free for 5 years at which time he developed intermittent cholangitis with an associated rise in bilirubin to 63 μmol/l and alkaline phosphatase to 558 U/l. Magnetic resonance cholangiopancreatography demonstrated dilatation of the anterior and posterior divisions of the right intrahepatic hepatic ducts (Fig. 3), following which he underwent percutaneous transhepatic cholangiography and dilatation of the portoenterostomy. He remained symptom free after this, but died of sepsis secondary to pneumonia 12 years after the initial operation. There was no evidence of recurrent disease and his liver function tests prior to death revealed a normal bilirubin (11 μmol/l) but an elevated alkaline phosphatase concentration (350 U/l), with no evidence of biliary dilatation on cross-sectional imaging.

Fig. 3
figure 3

Magnetic resonance cholangiopancreatography showing mild dilatation of the right-sided biliary tree up to the bilioenteric anastomosis (grey arrows) and an anastomotic stricture (white arrow)

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Patient 3

A 72-year-old man underwent a pylorus preserving pancreaticoduodenectomy for main duct intraductal papillary mucinous neoplasm with low-grade dysplasia. There was no preoperative evidence of bile duct dilatation. Reconstruction was undertaken using a retrocolic Roux-en-Y pancreaticojejunostomy, hepaticojejunostomy and antecolic gastrojejunostomy on a single jejunal limb. Two tube drains were left in the subhepatic and retrogastric spaces postoperatively. On the 5th postoperative day, the patient deteriorated acutely secondary to intraabdominal sepsis with associated hyperbilirubinemia (30 μmol/l). Cross-sectional imaging demonstrated a fluid collection with gas locules within the subhepatic space and areas of low attenuation within the right lobe of the liver consistent with arterial injury (Fig. 1). The subhepatic collection was drained percutaneously, confirming a biliary leak. Due to ongoing deterioration despite optimal medical management, the patient returned underwent surgical reexploration on the 12th postoperative day. At this time, the common hepatic duct stump was found to be ischemic to the level of the hepatic duct confluence with associated dehiscence of the hepaticojejunostomy. The pancreaticojejunostomy and gastrojejunostomy were intact. The existing hepaticojejunostomy was taken down and hepatic duct stump was resected to the level of the duct confluence. A retrocolic portoenterostomy was then constructed using interrupted 3-0 PDS across a 4 F feeding tube, with external peritoneal drainage via a tube drain. The patient remained on the ICU for 10 days and was eventually discharged from hospital 34 days after the original procedure. He represented 6 months later with cholangitis. Cross-sectional imaging demonstrated dilatation of the right-sided intrahepatic ducts, following which he underwent percutaneous transhepatic cholangiography and dilatation of the portoenterostomy (Fig. 4). Four years after the original procedure, the patient remains disease free with a normal serum bilirubin (19 μmol/l), an elevated alkaline phosphatase (446 U/l) with no intrahepatic biliary dilatation.

Fig. 4
figure 4

a Percutaneous transhepatic cholangiography using right-sided hepatic approach showing a contrast study via a previously placed percutaneous transhepatic biliary drain. There is an area of poor contrast flow through a strictured bilioenteric anastomosis (black arrow) with little contrast medium flowing into the Roux-en-Y jejunal loop (white arrow). b Percutaneous transhepatic cholangiography using right-sided hepatic approach. A significantly improved drainage of contrast medium into the jejunal loop is seen (white arrow) after a successful percutaneous transhepatic bilioenteric anastomotic dilatation using graded angioplasty balloons (black arrow)

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Discussion

End-to-side duct to mucosa hepaticojejunostomy is successful in up to 90% of patients,1 – 4 and major biliary complications occurring after hepaticojejunostomy that require surgical intervention are rare.6 The most common complications of hepaticojejunostomy are bile leaks (0.4–8%) and strictures (12–25%).6 – 8 These are more likely to occur when injury to the duct occurs close to the hepatic duct confluence or if there is a concurrent vascular injury. In most patients, hepaticojejunostomy-associated biliary complications can be managed with minimally invasive techniques.6 When surgical intervention is required, due to failed percutaneous intervention or refractory sepsis, reconstruction may still be undertaken by lowering the hilar plate to expose the hepatic duct confluence (the Hepp-Couinaud approach)9 – 13 or transecting the liver to expose viable intrahepatic ducts to which the hepaticojejunostomy can be sutured.12 , 14 – 16 When these approaches have failed, or are not feasible, reconstruction presents a challenge.

Portoenterostomy involves surgical anastomosis of the jejunum to a decapsulated area of the liver to establish a conduit from the intrahepatic bile ducts to the intestine.17 – 20 Originally described as a technique to treat congenital biliary atresia in infants, there are limited data on the use of portoenterostomy in adults.5 , 17 , 21 , 22

In the present series of three patients where portoenterostomy was used as a salvage procedure for major biliary complications following hepaticojejunostomy, we achieved long-term survival with relatively few symptoms. In each case, the original hepaticojejunostomy was undertaken for different indications but the resultant major biliary complications resulted in critically ill patients in whom minimally invasive techniques were not applicable and standard reconstruction using hepaticojejunostomy was not feasible due to the presence of small fragile ducts and systemic inflammation and sepsis.

Pickleman et al.20 described the use of portoenterostomy with transanastomotic stents in patients with bile duct injuries extending to the hepatic duct confluence (Bismuth type IV) following laparoscopic cholecystectomy. In this series of five patients, portoenterostomy was used successfully to restore biliary drainage, where standard reconstruction using hepaticojejunostomy was not feasible because of significant scarring and inflammation or the presence of small diameter separated hepatic ducts. Postoperatively, four of five patients required percutaneous transhepatic internal-external biliary stenting and dilatation for worsening liver function tests and biliary strictures.20 These stents were kept in situ for a variable length of time (9–25 months) with three monthly exchanges.20 Similarly, Mercado et al.23 performed portoenterostomies in 26 patients with Bismuth type IV injuries following laparoscopic cholecystectomy. At the time of operation, the right and left hepatic ducts were found separated and partially scarred and/or ischemic. Transhepatic transanastomotic stents were placed in nine patients and kept in situ for at least 6 months. Overall, 14 (53.8%) patients suffered from postoperative cholangitis, but the incidence of cholangitis in patients with or without transanastomotic stents was not statistically different (p = 0.075).23

Schlitt et al.24 used portoenterostomy to restore biliary drainage in three patients with chronic ischemic-type hepaticojejunostomy strictures following liver transplantation when no hepatic duct could be defined following resection of the ischemic stricture. In these patients, only transient improvements in biliary drainage were achieved, after which progressive deterioration in liver function necessitated retransplantation within a few months. This contrasted with 14 patients with chronic ischemic-type hepaticojejunostomy strictures where hepaticojejunostomy was feasible after resection of the ischemic stricture leading to a sustained improvement in biliary drainage.24

Gao et al.17 performed portoenterostomy with transanastomotic stents in ten patients with benign and malignant hilar strictures. Only one operation was complicated by a bile leak, which was managed conservatively. This approach achieved symptom-free survival in this heterogenous group of patients for up to 2 years.17

Previous studies have suggested that use of transanastomotic stents may reduce rates of anastomotic stricture in unfavourable conditions.13 , 17 , 20 , 25 , 26 The optimum duration of stenting is unclear. In our study, the stents were left in situ for 2 to 3 weeks after portoenterostomy and were removed once a contrast study confirmed the patency of the anastomosis and had excluded ongoing bile leak. The incidence of stricture formation at the site of portoenterostomy is uncertain in adults. In our series, two patients required percutaneous transhepatic cholangiography and dilatation of anastomotic strictures that developed months to years after the procedure. Long-term follow up of these patients is, therefore, necessary as late strictures may occur. In addition, there is no evidence about the efficacy of preoperative biliary stenting in such patients. In our patients, preoperative biliary stenting was precluded by the absence of dilatation of the intrahepatic duct on cross-sectional imaging and the fact that they were critically ill. However, if preoperative imaging confirms biliary dilatation and patient’s condition permits, preoperative percutaneous transhepatic biliary drainage could be considered, with the internal-external drains being allowed to traverse the anastomosis at the time of the operation. This approach may help in delineating biliary anatomy further and obviate the need for intraoperative transjejunal stents.

In conclusion, biliary reconstruction can usually be achieved by hepaticojejunostomy. In rare cases where hepaticojejunostomy is not feasible due to small, friable or inflamed hepatic ducts, portoenterostomy with transanastomotic stenting provides an effective way of saving life and restoring biliary drainage in patients with major biliary complications. Although this is not a procedure to be recommended without due consideration of other options, we have shown it can be life-saving and provide good long-term results in combination with postoperative radiological intervention, when necessary. The rarity of this operation is emphasized by the fact that we have had to perform only three such procedures in a tertiary referral centre over a 14-year period.