Endoscopic treatment and outcome-oriented classification of biliary strictures after liver transplantation: a multicenter retrospective cohort study

Introduction

Biliary complications after liver transplantation are a significant cause of mortality and graft failure (1-3). Biliary stricture (BS) is the most common type of biliary complication, with the highest reported incidence of 30% (4). Effective management of BS is crucial for improving patient prognosis (3). Stent implantation using endoscopic retrograde cholangiopancreatography (ERCP) is the preferred treatment option for BS (5). However, the imaging manifestations of BS are complex, and a standardized classification system is lacking. The stent treatment approach for BS also remains controversial.

A binary classification system based on the relationship between strictures and anastomoses was first applied to describe BS and is widely used. This system categorizes BS into anastomotic strictures (AS) and non-anastomotic strictures (NAS) (6). However, different studies use different definitions of NAS and AS, especially when the strictures are located within 0.5–1.0 cm proximal to the anastomosis, and some studies even define AS as only those located at the sites of anastomosis (2,7,8). Although the aforementioned binary classification has prognostic value, it does not contribute to treatment guidance given that treatment choices based on this classification are highly inconsistent (1).

Previous studies have attempted to effectively classify BS using various methods. Using a binary classification, Buis et al. further classified NAS (7). This complex classification method relies on comprehensive biliary imaging and subjective judgment by endoscopists, and there is currently insufficient evidence to demonstrate the value of the Buis classification in guiding treatment or predicting prognosis (9). Lee et al. classified intrahepatic BS into four types and reported statistically significant differences in prognosis among different types (10,11). However, this classification only focuses on the intrahepatic region and overlooks the overall nature of BS. Ling and den Dulk also established their own BS classification system (12,13). Both of these methods have not been widely used because they only describe strictures but fail to demonstrate their prognostic or therapeutic value. Kohli et al. performed an interobserver agreement study of several classifications, including the Ling, Lee and binary systems, and considered none of them to be suitable for describing BS at present (14). Park et al. recently proposed a classification system for intrahepatic BS in right lobe liver transplants and demonstrated its efficacy. However, the study’s target population determined the limitations of this model (15).

The Bismuth classification system has been widely applied in the assessment of biliary surgery. For endoscopic treatment, a BS classification system based on location that can guide treatment selection may be valuable but has not been validated before. The latest guidelines from the American Society for Gastrointestinal Endoscopy (ASGE) updated the recommendations for BS after liver transplantation (16). The guidelines provide treatment recommendations by distinguishing between intrahepatic and extrahepatic stenosis. The trend in treating BS depends on the highest stricture position within the biliary system. However, there are still no guidelines for intrahepatic and bifurcation strictures, especially for strictures involving hepatic confluence, and research data supporting such a system remain lacking.

Therefore, we retrospectively collected data from patients with BS who underwent stent implantation at three hospitals to develop a new classification system, providing clear treatment guidance for different types of BS. We present this article in accordance with the STROBE reporting checklist (available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-160/rc).

Methods

Study cohort

This was a retrospective, multicenter observational study across three centers (the First Affiliated Hospital of Army Medical University, the Third Affiliated Hospital of Naval Medical University and Nanjing Medical University Affiliated Jinling Hospital). All patients who underwent ERCP after liver transplantation between December 2015 and October 2022 were included. And all patients were included at the time of their first BS event. Patients who received living-donor transplantation and those who underwent ERCP procedures due to non-strictured factors were excluded.

All patients provided written informed consent for both undergoing ERCP at their respective institutions and participating in this study. This study was approved by the Institutional Review Board of the First Affiliated Hospital of Army Medical University (No. KY2023016) and the other two institutions were informed and agreed with this study. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

Data collection

Perioperative data, including recipient characteristics, transplantation operation data and perioperative complications, were retrospectively collected from the participating centers. ERCP images were evaluated by three experienced endoscopists. All patients included in the study did not receive mechanical perfusion treatment during transplantation. The following endoscopic treatment data were collected: diagnosis time of BS, characteristics of the stricture, features of ERCP treatment, perioperative complications, and laboratory parameters during the treatment period. Since this study was based on patient data collected from endoscopy centers, and these BS patients originated from various external transplant centers, we were unable to obtain transplant volume data or further graft-related parameters (including donor type).

Diagnosis and treatment

Patients were followed up after liver transplantation at their respective transplantation centers. When biliary obstructive symptoms or elevated laboratory parameters are identified, magnetic resonance cholangiopancreatography (MRCP) examination is performed. BS patients diagnosed using MRCP were subjected to an endoscopic procedure. Cholangioscopy is not employed as a routine diagnose approach for BS, and all enrolled patients have not received any treatment under cholangioscopy. All participating centers adopted stenting implantation rather than simple balloon dilation as the preferred treatment. The type of stent was selected autonomously based on the experience of different endoscopists. The experienced endoscopists at each participating center determined the stent treatment plan and performed the ERCP surgery. Balloon dilation or catheter dilation was only performed when the stent could not pass through the stricture before stent implantation. Patients were informed to undergo a repeat ERCP 3 months after plastic biliary stent (PBS) implantation or 6 months after fully covered self-expandable metal stent (FCMS) implantation. The combined FCMS + PBS implantation is typically performed in a noncoaxial manner and following three principles: (I) cholangiographic confirmation of stricture confinement to primary biliary ducts (left or right hepatic duct); (II) secondary duct bifurcation >1.5 cm distal to the hilar confluence (ensuring sufficient length for stent anchorage while preventing deep duct obstruction); (III) stepwise deployment: Non-coaxial PBS was first positioned in the contralateral duct, followed by FCMS implantation in the dominant stricture-bearing duct. Postoperative follow-up ERCP for FCMS + PBS is scheduled for 6 months postoperatively. The stent removal procedure is performed when patients meet the following criteria during hospitalization: absence of obstruction symptoms (abdominal pain, jaundice or itching), biochemical normalization and stricture relief under cholangiography.

Outcome

Outcomes were determined on the date of the last hospitalization or outpatient follow-up. Stent-free success was defined as a lack of stricture recurrence or new stricture development within 12 months after stent removal. Stricture recurrence refers to a second diagnosis of BS in patients who had undergone successful stent removal. Survival with a stent refers to patients within the stent indwelling period, including those who underwent stent reimplantation after recurrence. Loss to follow-up refers to patients who discontinued treatment due to non-BS-related factors.

BS classification

Patients were initially classified as having AS or NAS. NAS were defined as strictures located at a distance greater than 0.5 cm from the anastomosis. The new classification criteria were established by re-evaluating the images based on the highest position of involvement of the bile ducts in the initial successful ERCP images and dividing BS into three types (Figure 1). Type I refers to narrowing that occurs in the distal bile duct and is more than 2 cm away from the biliary bifurcation. This 2 cm threshold was determined based on the highest position for FCMS should maintain a sufficient distance from the bifurcation to prevent obstruction of contralateral intrahepatic ducts. Type I includes most AS and some NAS with lower anastomotic positions. Type II refers to narrowing that occurs in the common bile duct between 2 cm from the biliary bifurcation to the first-order branch and includes NAS located around the portal and AS with high anastomotic positions. Type III refers to narrowing at the opening of the second-order bile duct and the proximal intrahepatic bile ducts, and this category includes NAS with higher narrowing positions.

Figure 1 A novel ternary classification system for biliary transplantation after orthotopic liver transplantation (the red dotted circles indicate the stricture position). a, Single or multiple strictures of the intrahepatic bile ducts; b, Diffuse stenosis and rigidity of the intrahepatic bile ducts.

Statistical analysis

Continuous data were presented as the mean ± standard deviation and were compared using an unpaired two-tailed t-test, analysis of variance or Kruskal-Wallis test. Categorical variables were reported as numbers of cases and percentages and were assessed using the χ² test or Fisher’s test. Time-to-event curves were created using the Kaplan-Meier method, and differences were analyzed using the log-rank test. P<0.05 was considered to indicate statistical significance. All the statistical analyses were performed using R software (version 4.2.2; http://www.r-project.org/).

Results

Clinical characteristics of the included patients

During the study period, a total of 96 patients from three centers were included. The clinical characteristics of the patients are presented in Table 1. The mean age of the patients at the time of BS first diagnosed was 48.0±10.9 years, and there were 84 (87.5%) males and 12 (12.5%) females. Regarding primary disease, liver failure caused by hepatitis B virus infection was most common (51.0%), followed by liver tumors (32.3%), alcoholic cirrhosis (8.3%), autoimmune liver disease (3.1%), primary sclerosing cholangitis (1.0%) and others (4.2%).

Treatment choices for different categories

When BS was first diagnosed, 54 (56.3%) patients presented with AS, whereas 42 (43.7%) patients presented with NAS. After radiological re-evaluation, among the 96 patients, 42 (43.8%) were type I, 31 (32.3%) were type II, and 23 (24.0%) were type III. Stent treatment schemes used for the first successful endoscopic treatment were described based on these new classification methods (Figure 2A). Type I patients received FCMS treatment (61.9%) or single-PBS treatment (38.1%). Type III patients received only PBS, including single-PBS (30.4%) or multi-PBS (69.6%). However, patients with type II underwent a variety of treatment options, including multi-PBS (54.8%), FCMS + PBS (19.4%), single-PBS (16.1%) and FCMS (9.7%). To demonstrate the guiding significance of this new classification for treatment options, the stent treatment scheme used in the binary classification system was also described (Figure 2B). For patients with AS, FCMS (50.0%) and single-PBS (31.5%) were the main treatment options. In addition, 11.1% received multi-PBS, and 7.4% received FCMS + PBS. For patients with NAS, multi-PBS (66.7%) and single-PBS (23.8%) were the main treatment options, with 4.8% receiving FCMS and 4.8% receiving FCMS + PBS. Compared to the binary classification system, stent treatments in the new classification were more fixed, especially for type I and type III patients. Endoscopic images of the unique FCMS + PBS implantation scheme and the PBS implantation scheme used for type II patients are shown in Figure 3.

Figure 2 Stent type used during the first ERCP treatment. (A) Types of stents used under the new classification. (B) Types of stents used under the binary classification system. AS, anastomotic strictures; ERCP, endoscopic retrograde cholangiopancreatography; FCMS, fully covered self-expandable metal stent; NAS, non-anastomotic strictures; PBS, plastic biliary stent.

Figure 3 Two types of stent placement methods for type II patients. (A) BS before treatment; (B) multi-PBS implantation; (C) stricture remission after multi-PBS; (D) BS before treatment; (E) FCMS + PBS implantation; (F) strictures remission after FCMS + PBS. BS, biliary stricture; FCMS, fully covered self-expandable metal stent; PBS, plastic biliary stent.

Stent choices for different BS types

The treatment characteristics of FCMS + PBS and PBS were evaluated among type II patients (Table 2). The results indicated no significant differences between the two treatment groups in terms of operation time, stent duration or stent-free rate; however, the FCMS + PBS group had fewer stents implanted among patients who achieved stent-free success (P=0.02). In addition, although the cost per stent placement session with FCMS + PBS (29,853.4±5,303.8 CNY) was greater than that with multi-PBS (18,339.2±3,503.3 CNY, P<0.001), the lower number of treatment sessions made the total cost of FCMS + PBS (67,493.6±25,353.4 CNY) significantly lower than that of multi-PBS (89,012.8±14,039.2 CNY, P=0.04). For type I patients, Kaplan-Meier curves showed that the stent-free survival rate did not significantly differ between the FCMS and PBS groups (P=0.75) (Figure 4). Comparisons of the treatment characteristics revealed no significant differences terms of the stent-free rate, duration of stent placement, or incidence of complications between the FCMS and PBS groups (Table 3). However, among the patients who achieved stent-free status, the FCMS group underwent an average of 1.7±1.2 treatments, which was significantly lower than that of the PBS group (2.6±1.0, P=0.02). Similar to type II patients, the cost efficiency of FCMS treatment was also significantly lower than that of PBS treatment for type I patients (P=0.04).

Figure 4 Kaplan-Meier curves for time from initial ERCP to stent removal in type I patients. ERCP, endoscopic retrograde cholangiopancreatography; FCMS, fully covered self-expandable metal stent; PBS, plastic biliary stent.

Comparison of treatment characteristics and prognosis

The treatment characteristics of the different types are listed in Table 4. The average diagnosis time of all patients was 282.3±228.6 days after transplantation, and no significant difference was noted among the different types (P=0.69). The average durations of ERCP for types I, II, and III were 45.8±20.2, 51.5±22.1 and 55.6±19.2 minutes, respectively. A significant difference was noted among the three types, with type III having the longest surgical time and type I having the shortest (P=0.01). During the follow-up period, a total of 347 ERCP treatments were administered to 96 patients. Among them, type III had the highest number of ERCP procedures, whereas type II had the fewest. Significant differences were noted among the three types (P<0.001). The overall stent-free rate of the entire cohort was 58.3%, with 24% of patients still in the indwelling period. The stent-free rate was significantly greater for type I patients (69.0%) compared with type II (61.3%) and type III (34.8%) (P=0.03). Among patients who achieved stent-free success, type I patients required fewer treatment sessions and had a shorter stent duration (P<0.001 and P=0.04, respectively).

Kaplan-Meier curves were used to analyze the stent-free survival rate in patients who underwent surgery with different classification methods (Figure 5). Ninety-three patients were divided into two groups (green lines) and three groups (red lines) using binary classification and novel classification, respectively. The Kaplan-Meier curves showed no significant difference in the stent-free rate between type I and type II patients (P=0.15). Type I and type II patients had better stent-free rates than type III patients (P<0.001 and P=0.003). According to the binary classification, the stent-free survival rate of the AS group was significantly greater than that of the NAS group (P<0.001). Interestingly, there was no significant difference in stent-free survival between type I patients and AS patients or between type III patients and NAS patients. However, the stent-free rates of type II patients were not significantly different from those of AS patients but were significantly greater than those of NAS patients (P=0.046).

Figure 5 Kaplan-Meier curves for the time from initial ERCP to stent removal in patients among the different types of biliary stricture. AS, anastomotic strictures; ERCP, endoscopic retrograde cholangiopancreatography; NAS, non-anastomotic strictures.

Discussion

To our knowledge, this is the first study to classify BS after liver transplantation based on the highest position of strictures and treatment selection. In this multicenter retrospective study, we established a novel tripartite classification method in which the three types had well-defined boundaries based on the treatment characteristics. Specifically, compared to PBS, FCMS for type I patients and FCMS + PBS for type II patients served as superior treatment modalities, demonstrating lower costs and shorter treatment durations. With the increasing application and recognition of FCMS in the treatment of BS, this location-based classification conforms to the current treatment trend (16-19). Patients also exhibit differences in prognosis based on this novel classification system.

According to the latest guidelines for the management of post-liver transplantation biliary stricture (LTBS) issued by the ASGE, FCMS placement was recommended as the preferred choice for extrahepatic BS, regardless of whether the stricture was located at the anastomosis site (16,17). This finding suggested that the most widely used traditional binary classification method does not provide guidance for treatment. Depending on the transplantation procedure and biliary reconstruction method used at different centers, the anastomosis sites range from immediately below the bifurcation to the farthest distal bile duct (4,6,20). This variation makes binary classification ineffective as a useful method for guiding treatment.

According to the latest American College of Gastroenterology (ACG) guidelines for BS, strictures are classified into three types based on concrete implications in the approach to diagnosis and drainage: extrahepatic, perihilar, or intrahepatic (21). However, this concept requires more research and assessment in the setting of post-liver transplant BS. To avoid blocking bile drainage on one side, a single FCMS is considered unsuitable for strictures within 2 cm of the hepatic confluence (22,23). We believe that this serves as a good demarcation point to differentiate BS, and different classifications can effectively guide the selection of stents. For type I patients, both FCMS and PBS were the main treatment choices in previous studies (5,24). Several studies have demonstrated the advantages of using FCMS for extrahepatic BS. This finding is also confirmed in this study. Consistent with the ASGE guidelines, we recommend FCMS as the preferred treatment for type I patients.

On the premise that an extrahepatic BS with a hepatic confluence of greater than 2 cm is defined as type I, perihilar BS should be regarded as another independent type that differs from intrahepatic BS. Because the high position of the perihilar BS is not suitable for implantation of the FCMS alone, we attempted to insert the FCMS across the narrowed segment, extend it into the left hepatic duct, and insert the PBS on the other side to prevent obstruction (Figure 3F). Notably, this patient did not experience any complications after this procedure and demonstrated a good treatment response during 6 months of follow-up. For five patients who received FCMS + PBS implantation, this treatment showed excellent therapeutic effects. In previous studies, the combined use of FCMS and PBS has been shown to reduce the incidence of complications associated with FCMS (25). In this study, compared with PBS, FCMS + PBS resulted in fewer treatment sessions and lower treatment costs for type II patients. We believe that this is a potentially effective treatment because the FCMS extends beyond the hepatic confluence and the stricture segment, whereas the PBS is inserted into the contralateral secondary bile duct. However, due to the limited number of patients, the effectiveness and safety of this approach still need to be verified in a larger sample. The boundary between type II and type III is the opening of the secondary bile duct, as FCMS cannot be implanted for further treatment.

PBS remains the only stent implantation choice for type III patients at present, and intrahepatic BS has been associated with a poor prognosis (3,26). Based on the prognostic analysis of this study, patients with type III also demonstrated the poorest prognosis. Although endoscopists have made efforts to achieve adequate drainage at narrowed sites, the treatment outcome for intrahepatic BS remains uncertain due to their complex radiological manifestations. It is necessary to further divide type III into subtypes based on their narrow characteristics. Lee et al. classified intrahepatic BS according to imaging manifestations and reported good results for prognostication (11). Although both strictures occur in the intrahepatic bile ducts, the prognosis of the bilateral multifocal type is significantly better than that of the diffuse necrosis type (10). Therefore, we also propose subdividing type III into type IIIa and type IIIb. Although its poor prognosis suggests that re-transplantation is the ultimate treatment option for type IIIb patients, stent drainage is still worth attempting. Furthermore, although this study suggests that stent placement is a more effective therapeutic approach, balloon dilation of strictures may hold potential therapeutic value prior to stent implantation and for distal intrahepatic bile ducts where stent placement is technically challenging, particularly in type III cases. In terms of prognosis assessment, this novel classification method also demonstrated excellent performance. Type I and type II patients showed similar stent-free rates, with both groups displaying higher rates than those noted for type III patients. Interestingly, in Park et al.’s study, the involvement of secondary bile ducts in NAS did not lead to a significant decrease in graft survival compared to AS, and the poorer prognosis in patients with this disease is attributed to more distal intrahepatic bile duct strictures (15). Our results further corroborate this finding, indicating that although some type II patients present with NAS, their prognosis is better than that of patients with strictures above the secondary bile ducts. The stent-free survival rate of type II patients was significantly better than that of NAS patients. Compared to binary classification, we believe that this ternary classification method is more meaningful for assessing patient prognosis.

The scope of this classification includes the entire reconstructed biliary system, encompassing both the transplanted hepatic ducts and the recipient bile ducts. Clear demarcation points make the classification of BS easy to determine. In addition, this approach provides a potential FCMS-based treatment scheme for type II strictures. Nonetheless, this study has several limitations. First, the retrospective design inevitably introduces selection bias and partial missing follow-up data. Second, the factors influencing BS prognosis are multifaceted, with the treatment regimen being only one component. Further determination of the impact of treatment regimens on prognosis requires the integration of established risk factors, such as the time of diagnosis and biliary duct compatibility, to enable a comprehensive assessment. Third, although this study is based on multicenter data, after classification, the sample size for each type was small, making further subgroup analysis to refine the classification difficult to achieve. Therefore, larger-scale studies are needed to validate the rationale for FCMS + PBS treatment methods for type II patients and to further subtype type III patients. Fourth, the interobserver consistency of this new classification system has yet to be confirmed.

Conclusions

In conclusion, we established a location-based ternary classification system for BS after liver transplantation. This new classification system can evaluate the whole biliary tract, providing valuable treatment guidance and prognosis assessment. It represents an effective classification approach with promising clinical applications.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-160/rc

Data Sharing Statement: Available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-160/dss

Peer Review File: Available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-160/prf

Funding: This work was supported by Chongqing Technology Innovation and Application Development Special Key Project (No. CSTB2022TIAD-GPX0085).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-160/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 patients provided written informed consent for both undergoing ERCP at their respective institutions and participating in this study. This study was approved by the Institutional Review Board of the First Affiliated Hospital of Army Medical University (No. KY2023016) and the other two institutions were informed and agreed with this study. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

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/.

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