The role of Roux-en-Y hepaticojejunostomy for the management of biliary complications after living donor liver transplantation
BMC Surgery volume 23, Article number: 165 (2023)
Post living donor liver transplantation (LDLT) biliary complications can be troublesome over the post-operative course of patients, especially those with recurrent cholangitis or choledocholithiasis. Thus, in this study, we aimed to evaluate the risks and benefits of Roux-en-Y hepaticojejunostomy (RYHJ) performed after LDLT as a last option to deal with post-LDLT biliary complications.
Retrospectively, of the 594 adult LDLTs performed in a single medical center in Changhua, Taiwan from July 2005 to September 2021, 22 patients underwent post-LDLT RYHJ. Indications for RYHJ included choledocholithiasis formation with bile duct stricture, previous intervention failure, and other factors. Restenosis was defined if further intervention was needed to treat biliary complications after RYHJ was performed. Thereafter, patients were categorized into success group (n = 15) and restenosis group (n = 4).
The overall success rate of RYHJ in the management of post-LDLT biliary complications was 78.9% (15/19). Mean follow-up time was 33.4 months. As per our findings, four patients experienced recurrence after RYHJ (21.2%), and mean recurrence time was 12.5 months. Three cases were recorded as hospital mortality (13.6%). Outcome and risk analysis presented no significant differences between the two groups. A higher risk of recurrence tended to be related to patients with ABO incompatible (ABOi).
RYHJ served well as either a rescue but definite procedure for recurrent biliary complications or a safe and effective solution to biliary complications after LDLT. A higher risk of recurrence tended to be related to patients with ABOi; however, further research would be needed.
Living donor liver transplantation (LDLT) had gained popularity over the recent decades and proved to be as curative as deceased donor liver transplantation (DDLT) . However, the presence of biliary complications remain as an insurmountable difficulty in terms of LDLT, especially those receiving a right lobe liver graft .
Post-LDLT biliary complication rate can vary between centers and countries, ranging from 9.6% to 19% [3,4,5,6]. Efforts taken to minimize post-LDLT biliary complications had evolved over the years. Prevention of local ischemia of biliary tract and preceding bile leakage might contribute to reducing post-operative risk of biliary anastomosis stricture [7, 8]. Intraoperatively, technical modifications of choledochocholedochostomy helped improved the stricture rate. A theoretically higher risk of biliary tract ischemia was suggested of an end-to-end anastomosis as it added fragility and an impaired perfusion at the distal end of the bile duct [8, 9].
However, with the nature of graft and possibility of rejection, a certain percentage of patients were still found to be at high risk of post-LDLT biliary complications [7, 8]. The necessity of managing such conditions was challenging yet inevitable. With the progress of techniques and equipment over the recent years, endoscopic maneuvers had largely replaced the role of surgical intervention while dealing with biliary complications after LDLT . Percutaneous transhepatic drainage (PTCD) also gained popularity for it served as a second-line management for patients who were treated with endoscopy yet deemed unsuccessful or those who were not suitable to receive an endoscopic procedure.
The above endoscopic techniques could help out almost 80% of the patients suffering from post-LDLT biliary complications , with varying success rates from 53 to 88% . Some patients may experience procedure failure probably due to a sharp angle of the biliary tract or severe stenosis. Intrahepatic duct (IHD) stones formation might also lead to recurrent cholangitis. A rescue percutaneous treatment could temporarily relieve obstructive jaundice or cholangitis and prevent progression of infection. However, drainage tube may cause inconvenient to the patient and may not thoroughly solve bile duct stricture. Under such circumstances, re-anastomosis of the biliary-enteric route seemed to be necessary. A Roux-en-Y hepaticojejunostomy (RYHJ) is the choice of surgical method [13,14,15,16]. The aim of this study is to evaluate the safety and recurrence risk factors of RYHJ performed after LDLT as a last resort of dealing with post-LDLT biliary complications.
Materials and methods
Between July 2005 and September 2021, 594 patients who had underwent LDLT were retrospectively recruited from Changhua Christian Hospital in Taiwan. Patients between 18 and 85 years old with a living donor right lobe graft and subsequently RYHJ were enrolled into this study. Exclusion criteria include patients whose ages were under 18 years old or over 85 years old at the time of operation. Among the 22 patients identified, 3 were excluded due to hospital mortality. In total, 19 patients met the inclusion criteria and were enrolled in this study for outcome and risk factor analysis (Fig. 1). Restenosis was defined if further intervention was needed to treat biliary complications after RYHJ was performed. Patients were then categorized into the success group (n = 15) and restenosis group (n = 4). This study was approved by the Institutional Review Board of Changhua Christian Hospital, Changhua, Taiwan.
The recipient surgery technique was mentioned in previous published literature .
Post-LDLT RYHJ was performed by a single surgeon. A right subcostal incision was made with a midline extension to the xiphoid. The adhesive bowel and stomach were lysed from the liver in order to locate and expose the liver hilum well. During hilar adhesion lysis, we paid extra attention toward the dissection of the hepatic artery (HA). After carefully identifying the HA and the common bile duct (CBD), cavitational ultrasonic surgical aspirator was applied to dissect the liver parenchyma around the graft right IHD. The previous right IHD – common hepatic duct anastomosis was identified and resected. Roux limb was designed from proximal jejunum. The anastomosis of hepaticojejunostomy was done in a fashion of continuous suture of the posterior wall and interrupt suture of the anterior wall. Moreover, 6–0 monofilament, nonabsorbable polypropylene sutures were used for the anastomosis. We enveloped the Glissonean sheath of the graft right IHD to the anastomosis to prevent early bile leak. While performing the anastomosis, a nasogastric tube or T-tube was often used as an intra-ductal stent. The choice of the size of tube depends on the diameter of graft right IHD measured intraoperatively. Drainage tubes were placed over Morison pouch and left subphrenic space.
Patient demographic data was retrospectively gathered from each patient. The age, gender and Model for End-Stage Liver Disease (MELD) score were recorded during history taking on admission for operation or chart record review. Operational-related data were extracted from operative records. The presence of rejection was defined as post-operative administration of bolus corticosteroid. The diagnosis of bile leak was made with biloma formation noted on contrast computed tomography or contrast leakage noted on cholangiogram or cholangioscopy. Intrahepatic duct stone was based on the finding of computed tomography or filling defects noted on cholangiogram or cholangioscopy . Patients were followed up until March 2022. Recurrence was defined if further intervention was needed to treat biliary complications after RYHJ was performed.
All of the above data were reviewed and confirmed by two of the researchers of this literature.
Quantitative data are expressed as means and standard deviations, whereas categorical variables are summarized as numbers and percentages. The Pearson chi-square (Fisher) test and Mann–Whitney U test were used to examine differences in demographic and clinical characteristics within the two groups. A p-value lower than 0.05 was statistically significant in our analysis. All statistical analyses were performed using IBM SPSS Statistics, version 22.0.
From July 2005 and September 2021, 594 patients underwent LDLT in our center. The mean age of the patients receiving RYHJ was 52.53 ± 6.04 years old. Clinical and operative characteristics of patients of LDLT who underwent subsequent RYHJ were listed individually in Table 1. Summative data analysis was listed in Table 2.
Recurrence risk and outcome analysis
Nineteen out of the 22 patients from the patients of LDLT who underwent subsequent RYHJ and didn’t experience hospital mortality were enrolled for recurrence risk and outcome analysis. Overall, the success rate of RYHJ in managing post-LDLT biliary complications was 78.9% (15/19). Mean follow up time was 33.4 months. Four patients experienced recurrence after RYHJ (21.2%), and mean recurrence time was 12.5 months. Comparing the group of patients who suffered from biliary complication recurrence and those who did not, no variable was proved to be a significant risk factor regarding recurrence after RYHJ. Comparisons of demographic data and clinical features of between patients with and without restenosis were listed in Table 3.
Three cases were recorded as hospital mortality, where in one of them suffered from HA injury intraoperatively during RYHJ; soon complicated with early bile leak, the patient expired due to subsequent sepsis. The other two patients had severe infections after endoscopic interventions and underwent RYHJ, yet multiple organ failure developed for malicious systemic infection and both of them expired.
During long-term follow-up, five patients expired in the non-recurrence group, and all other patients were currently under regular outpatient follow up. Among them, two patients suffered from hepatocellular carcinoma recurrence; one died due to metastatic obstructive pneumonia; one had aortic stenosis and underwent aortic valve replacement, yet the patient expired due to post-operative myocardial rupture; and one passed away for esophageal varicose bleeding with hepatorenal syndrome. The average follow-up time for those expired was 20.7 months.
Post LDLT biliary complications is an issue commonly discussed yet still not fully understood, especially those with a right lobe liver graft [17,18,19]. Even with advanced equipment and improved techniques, a certain percentage of patients still might not be thoroughly managed with non-operative interventions. The high failure rate of LDLT patients may be due to small-caliber bile duct anastomosis and multiple and more complex fibrotic anastomoses; it can also be attributed to liver graft hypertrophy . Under certain circumstances, RYHJ seemed to be the last resort in terms of dealing with post-LDLT biliary complications . Hepaticojejunostomy for biliary tract obstruction following liver transplantation was recommended for patient with endoscopic intervention failure. Also, the surgical procedure provided a more effective way in the management of cases with complicated biliary complications, such as necrosis of the bile duct, IHD stones, or extensive biliary leakage, since its procedural steps help established a thorough view of the major biliary system and biliary concrements can be extracted by flushing all major bile ducts under direct visualization .
Our study focused on these patients who suffered from either non-operative intervention failure or other clinical conditions not suitable for endoscopic or radiologic interventions (i.e., choledocholithiasis, acute bleeding, septic shock, etc.) The biliary-enteric anastomosis may provide an eternal solution to difficult shaped CBD or non-anastomotic biliary strictures [8, 10]. According to previous analysis, the overall success rate of our study was 78.9% (15/19). Four patients experienced recurrence after RYHJ (21.2%), and mean recurrence time was 12.5 months. Another center reported their experience with 16% of complication rate and 11% of restenosis rate . Chok. et al. published a series of studies on RYHJ managements after LDLT, proving a promising overall success rate with 76% [16, 20, 21] and thus making surgical managements of post-LDLT a salvaging last resort. They also suggested that side-to-side RYHJ could be a more suitable choice over side-to-end anastomosis, for the previous could reduce the chance of HA injury and allow a better chance for post-operative endoscopic procedure . In post-orthotopic liver transplantation RYHJ, a high-volume single center provided their experience with a mean survival rate of 70% and a 5-year survival rate of 68%, proving it as a promising rescue procedure for post-liver transplantation biliary obstruction not resolved by endoscopic procedures .
Three patients were recorded as hospital mortality in our analysis. One of the patients suffered from HA insufficiency postoperatively, even after stent placement. The patient developed intrahepatic biloma and subsequent liver failure. We recognized HA insufficiency may be a troublesome condition to deal with in post-LDLT RYHJ. Two of the patients underwent the surgery after intra-abdominal infection developed due to multiple failure episodes of endoscopy. We hence would like to suggest that RYHJ should be performed right after non-surgical intervention has failed. Mortality rate of post-LDLT RYHJ tended to be higher if the patient was presented with pre-operative infection.
Recurrence of biliary complications after RYHJ seemed to be frustrating yet inevitable (Fig. 2a). Recurrent IHD stones or restenosis of the more upstream biliary tree (e.g., right posterior branch) was observed in these patients even after RYHJ was performed. Although non-significantly, we noted a relative higher percentage of ABOi in patients with biliary complication recurrence after RYHJ. In current clinical practices, a standardized desensitization protocol with anit-CD20 antibody (rituximab) and plasma exchange had proved its ability of providing a comparable outcome for adult LDLT recipients receiving an ABOi graft [8, 22,23,24,25]. Despite that, the incidence of biliary complications still remained higher than ABO-compatible patients , ranging from 12.4%  to 50% . RYHJ may not be a definite treatment for ABOi patient who suffered from post-LDLT biliary complications, for ABO antigens were found on bile duct epithelium and might cause continuous intrahepatic bile duct injury due to immune response activation [8, 28]. As we review the pre-operative antigen titer before plasma exchange, those with recurrence aren’t higher. During follow-up, the concentration of tacrolimus and antigen titers is all within acceptable range according to chart records. This may suggest the possibility of episodes of subclinical inflammations in these patients due to persisted biliary epithelial injury and thus the failure of RYHJ. A relative higher percentage of female patients was noted in the restenosis group. Previous literatures rarely reported gender as a significant risk factor for biliary complications in liver transplantation [29, 30]. Verdonk et al. reported that female donor/male recipient pair was a significant risk factor post-transplantation anastomosis stricture. However, sex mismatch had only been reported as a risk of chronic rejection and failure of the graft , and our data discrepancy might be caused by a small number of case and data bias.
Among the four patients with symptomatic recurrence after RYHJ, we arranged PTC drainage (Fig. 2b) and subsequently a three-episode balloon dilatation protocol for most of them (Fig. 2c). The average time of protocol initiation was 47.8 months after RYHJ, immediately after biliary stricture was diagnosed. To date, all of the patients who received this protocol were currently free from symptomatic biliary complications.
This study has limitations. Although our case number was comparable to other literatures, it is still a rather small size cohort. Selection restriction was inevitable for there’s a significant difference in operative indications between early and late RYHJ patients. This may indicate a fundamental distinction between the two groups of patients. Analysis bias could possibly be presented considering such circumstances.
RYHJ served well as either a rescue but definite procedure for recurrent biliary complications or a safe and effective solution to early biliary complications after LDLT. We reported that none of the factor was proved to be a recurrence risk factor regarding the failure of RYHJ after LDLT for biliary stenosis managements. Although non-significantly, a relatively higher percentage of recurrence seemed to be related to patients with ABOi.
Availability of data and materials
The data that support the findings of this study are available from Changhua Christian Hospital, but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data are however available from the authors upon reasonable request and with permission of Changhua Christian Hospital.
Living donor liver transplantation
Deceased donor liver transplantation
Percutaneous transhepatic drainage
Common bile duct
Model for End-Stage Liver Disease
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None of the authors have conflicts of interest or financial ties to disclose.
Ethics approval and consent to participate
All methods were carried out in accordance with relevant guidelines and regulations, and this study was approved by the Institutional Review Board of Changhua Christian Hospital as No. 211025 of Institutional Approval Certificate of Human Research. Informed consent was obtained from all subjects and/or their legal guardian(s).
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Wen, TC., Hsieh, CE., Hsu, YL. et al. The role of Roux-en-Y hepaticojejunostomy for the management of biliary complications after living donor liver transplantation. BMC Surg 23, 165 (2023). https://doi.org/10.1186/s12893-023-02052-0