Endoscopic management of biliary leaks: a systematic review with meta-analysis

• Abstract
• Introduction
• Description of the condition
• Description of management
• Why it is important to do this review
• Methods
• Inclusion and exclusion criteria
• Search strategy
• Data extraction
• Quality assessment
• Data analysis
• Results
• Description of studies
• Patients
• Interventions
• Randomized clinical trials
• Prospective cohort studies
• Outcomes
• Quality assessment
• Randomized clinical trials (Fig. 2 and Appendix 3s)
• Prospective cohort studies (Appendix 3s)
• Effects of interventions
• Sphincterotomy alone vs. stenting alone vs. sphincterotomy with stenting
• Small-diameter stents vs. large-diameter stents
• Refractory biliary leaks
• Low grade vs. high grade leaks
• NBD
• Discussion
• References

Abstract

Background The first-line approach to the treatment of biliary leaks is endoscopic retrograde cholangiopancreatography. A variety of techniques can be used, including sphincterotomy, stenting, a combination of both techniques, or nasobiliary drainage. We performed a systematic review with meta-analysis to define the optimal strategy.

Methods We searched MEDLINE/PubMed, EMBASE, CENTRAL, Scopus, Google Scholar, and Web of Science until January 2018 for randomized clinical trials, case-control studies, and prospective cohort studies. Data on procedure, success, and complication rate were extracted. Risk of bias was assessed. A network meta-analysis was performed to compare sphincterotomy alone vs. stenting alone vs. combination treatment. Stenting was further stratified into leak-bridging and short stenting.

Results 11 studies out of 5085 references were included. Compared with sphincterotomy alone, the combination of sphincterotomy with leak-bridging stenting had the highest success rate (risk ratio [RR] 1.15, 95 % confidence interval [CI] 0.97 – 1.50), followed by leak-bridging stenting alone (RR 1.10, 95 %CI 0.84 – 1.44). For nonbridgeable leaks, stenting alone had a higher success rate than sphincterotomy alone (RR 1.07, 95 %CI 0.72 – 1.40). The combination of short stents with sphincterotomy had no added benefit (RR 0.94, 95 %CI 0.49 – 1.29). Overall quality of the included studies was considered to be moderate.

Conclusions We recommend sphincterotomy with stenting if the biliary leak can be bridged. If not, stenting alone with a short stent may be preferred in order to avoid sphincterotomy-related complications. More and larger studies are needed to confirm these findings.

Introduction

Description of the condition

Biliary leaks most commonly occur as a surgical complication, especially after (laparoscopic) cholecystectomy, liver transplantation, or partial liver resection [1]. The majority of biliary leaks are not detected during the surgical interventions and are only recognized after a significant delay owing to the nonspecific clinical presentation [2] [3]. However, rapid clinical deterioration may be seen as a result of peritonitis and sepsis. Early diagnosis and prompt management are therefore of utmost importance.

Description of management

Management of biliary leaks requires a multidisciplinary approach, with hepatobiliary surgeons, interventional radiologists, and endoscopists [4]. The first-line approach is endoscopic retrograde cholangiopancreatography (ERCP) [5] [6]. The goal is to decrease the transpapillary pressure gradient, allowing preferential flow of bile into the duodenum rather than extravasation at the leak site [7]. This can be achieved through a variety of endoscopic techniques, of which biliary sphincterotomy, biliary stenting or a combination of both techniques are most commonly used.

Why it is important to do this review

The optimal endoscopic treatment of biliary leaks is still controversial. Early studies suggested that sphincterotomy may be more successful than stenting [8] [9]. More recent studies, however, suggest that sphincterotomy might be inferior to stenting [5] [10]. Alternative techniques, such as nasobiliary drainage (NBD), have also been described. However, despite potential advantages such as the application of suction to decompress the biliary system, these drains require longer hospitalization, are not well tolerated, and accidental dislodgment is frequent [11] [12].

The optimal length and diameter of the inserted plastic biliary stents have also been debated. Some groups advocate the use of leak-bridging stents (when possible), while others use short stents (i. e. transpapillary stents that do not bridge the leak) [7] [13]. Most endoscopists favor large-diameter stents, although recent studies doubt the importance of stent diameter [14] [15]. Large and refractory biliary leaks are sometimes treated with multiple plastic stents (MPS) or fully covered self-expandable metal stents (FCSEMS) [16] [17]. Biliary stent removal is usually performed after 4 – 8 weeks.

To date, no systematic review/meta-analysis has been performed to define the best strategy for endoscopic management of biliary leaks in daily clinical practice. We aimed to address the following questions.

1. Should we perform sphincterotomy, stenting, or a combination of both techniques as the first-line treatment for biliary leaks?

2. Should we aim to bridge the biliary leak with stents?

3. What stent diameter should be used?

4. Is NBD an appropriate option?

5. How should we deal with biliary leaks that are refractory to first-line endoscopic management?

Methods

Inclusion and exclusion criteria

Eligibility criteria were formed a priori using the PICO model and are listed in [Table 1]. The model identifies the population, interventions, type of studies, and outcomes. Studies comparing different endoscopic techniques for the management of biliary leaks were included.

Search strategy

A systematic review was completed according to the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) and the Meta-analyses Of Observational Studies in Epidemiology (MOOSE) guidelines (see Appendix 1s in the online Supplementary material) [18] [19]. In January 2018, we searched MEDLINE/PubMed, EMBASE, CENTRAL, Scopus, Google Scholar and Web of Science using the following search terms: “biliary leak,” “endoscopic retrograde cholangiopancreatography,” “ERCP,” “sphincterotomy,” “stent,” and “nasobiliary drainage.” Search strategies are given in Appendix 2s. We manually scanned the reference lists of the included trials to identify additional trials of interest.

Data extraction

The review author K.V. considered trials for inclusion. The obtained references were first screened by title and abstract before full-text screening was performed where appropriate. In case of doubt about eligibility, the final decision for inclusion or exclusion was made after discussion with a second author (P.H.). Extracted data (according to availability) included all relevant information to assess the treatment outcomes and risk of bias. Additional data extraction included demographic details, setting, grade and site of the leak, interval between operation and endoscopic procedure, and period of follow-up. Authors were contacted through email in case of lack of data.

Quality assessment

We followed the instructions given in the Cochrane Handbook for Systematic Reviews of Intervention for the risk of bias analysis of the included randomized clinical trials [20]. The methodological quality of the nonrandomized clinical trials was assessed using the Newcastle-Ottawa scale [21].

Data analysis

Success rates of the endoscopic procedures across all included studies were calculated. For dichotomous variables, we calculated relative risk ratio (RR) and odds ratio (OR) with a 95 % confidence interval (CI). For continuous data, the medians with standard deviations were used to calculate effect differences and 95 %CIs.

A network meta-analysis was performed in R using the patient-centered network meta-analysis package (https://CRAN.R-project.org/package=pcnetmeta) to compare the main treatment groups (sphincterotomy alone, stenting alone [leak-bridging or short stents], combination of sphincterotomy with leak-bridging or short stents) [22]. This package uses Markov chain Monte Carlo (MCMC) algorithms to estimate parameters on the R platform through JAGS, which is a program for analyzing Bayesian hierarchical models. An inverse-Wishart was assigned prior to the variance – covariance matrix of random effects, 200 000 iterations were performed for adaptation to maximize sampling efficiency and 200 000 iterations in each MCMC chain.

Results

Description of studies

We identified a total of 5085 references through electronic searches of MEDLINE/PubMed (n = 806 hits), EMBASE (n = 1683), CENTRAL (n = 79), Scopus (n = 1709), Google Scholar (n = 51), and Web of Science (n = 757), of which 11 studies were suitable for inclusion [16] [23] [24] [25] [26] [27] [28] [29] [30] [31] [32]. Four studies were randomized clinical trials and seven were prospective cohort studies ([Fig. 1]). Nine studies were full-text journal articles and two were published abstracts [23] [24]. Details of the included studies are shown in Appendix 3s.

Patients

The number of patients in each trial ranged from 13 to 207. Age varied from 18 to 95 years. About 60 % of study patients were women.

Most studies dealt with biliary leaks after cholecystectomy. One study reported treatment of biliary leaks after liver transplantation, and another reported on biliary leaks after partial liver resection [25] [26]. In two other studies, all leaks were included irrespective of their cause, but cholecystectomy turned out to be the main cause (85 % and 91 %, respectively) [23] [24].

In the studies after cholecystectomy, bile leakage was mostly found at the site of the cystic duct stump (65 %), followed by the common hepatic duct/common bile duct (14 %), and the duct of Luschka (13 %).

The severity of leak was described in four studies [16] [24] [27] [28]. A leak was considered low grade (leak identified only after intrahepatic opacification) or high grade (leak observed before intrahepatic opacification) in 48.5 % and 51.5 %, respectively.

The interval between operation and endoscopic intervention varied from 1 week to 4 months. However, ERCP was mostly performed in the second week after the operation (mean interval 8.7 days).

Interventions

Randomized clinical trials

There were four randomized clinical trials, involving 183 patients [16] [23] [29] [30]. There was no statement of a power analysis having been performed.

Two trials (41 and 27 patients, respectively) compared sphincterotomy with stenting [23] [29]. One trial (52 patients) investigated the need to perform an additional sphincterotomy if patients were treated with stent placement [30]. The fourth randomized trial was a comparative study of 7 Fr vs. 10 Fr stents [16].

Prospective cohort studies

There were seven prospective cohort studies, involving 477 patients [24] [25] [26] [27] [28] [31] [32].

Concerning the studies after cholecystectomy (361 patients), the interventions performed were heterogeneous. Barton et al. [31] compared sphincterotomy alone with stenting after sphincterotomy, whereas Agarwal et al. [32] compared four groups (sphincterotomy and stenting, sphincterotomy and NBD, stenting alone, and NBD alone). Sandha et al. [27] investigated a systematic approach in which low grade leaks were treated with sphincterotomy, whereas stenting after sphincterotomy was used in high grade leaks. Canena et al. [28] compared the use of an FCSEMS with the placement of MPS for the treatment of refractory biliary leaks. Refractory biliary leaks are those that fail to respond (persistent high output from percutaneous drain or persistent leak at cholangiography) to a plastic stent and biliary sphincterotomy for more than 2 weeks [28] [33].

Chandra et al. [24] examined all kinds of biliary leaks (68 patients) and compared sphincterotomy alone vs. sphincterotomy with stenting. The study by Liao et al. [25] in patients (n = 13) who had undergone liver transplantation compared stenting, sphincterotomy, and NBD. Finally, Schaible et al. [26] compared sphincterotomy alone vs. sphincterotomy with stenting for leaks after partial liver resection (35 patients).

Outcomes

All trials reported clinical success of the endoscopic procedures. Failure of the endoscopic procedure was defined as persistence of biliary output through the percutaneous drains (after 3 – 7 days, although this was inconsistently defined) and/or the persistence of the biliary leak at follow-up ERCP or cholangiography, requiring reintervention, including repeat ERCP or surgery.

Time to leak closure was described in five studies including two randomized trials [23] [24] [28] [29] [32]. A mean value of the duration of hospital stay was reported in only one study [24]. All but one study [24] described mortality and morbidity outcomes. However, in three studies [23] [26] [27], data were only reported for the entire patient group, making it impossible to compare the different intervention groups. Morbidity referred to complications from ERCP procedures, such as pancreatitis, cholangitis, hemorrhage, and perforation.

Quality assessment

Randomized clinical trials ([Fig. 2] and Appendix 3s)

There was no blinding in any of the included trials. Owing to the nature of the interventions, blinding of the participant (e. g. stent removal needed after 4 – 8 weeks) and endoscopist is not possible. Trials could have used blinded outcome assessors.

Only one trial reported the use of computer-generated random number sequences and was therefore at low risk of selection bias [16]. In two trials, the sealed envelope method was used [16] [30]. In all but one trial, the outcome data were complete. The trial by Dolay et al. was at high risk of attrition bias as it excluded two patients in the sphincterotomy group because they underwent stenting following failure of leak closure [29]. All included trials were considered to be at low risk of reporting bias, with the exception of one study in which the risk of bias was considered unclear, as the time to leak closure was described for all patients (no different values for the two groups) [30]. The risk of other potential sources of bias was considered to be low in all studies except one, in which the risk was considered unclear as the data were from a published abstract [23].

Prospective cohort studies (Appendix 3s)

The methodological quality of five of the seven prospective cohort studies was rated as Grade A (score 7 – 9, high quality). The other two studies were rated as Grade B (score 4 – 6, medium quality), mainly due to lack of comparability of the groups and insufficient follow-up [25] [27].

Effects of interventions

Sphincterotomy alone vs. stenting alone vs. sphincterotomy with stenting

Data from all studies were used for this comparison, except for one, in which only refractory biliary leaks were treated [28]. In each of the included studies, one (Katsinelos et al. compared two types of stents) or more of these interventions were compared. Interventions were subdivided into five main groups: 1) sphincterotomy alone, 2) stenting with leak-bridging stents, 3) stenting with short stents, 4) sphincterotomy with leak-bridging stenting, and 5) sphincterotomy with short stenting.

All studies reported on the clinical success of the endoscopic procedures. The success rates in the five main groups were 90.5 %, 95.6 %, 91.4 %, 98.3 %, and 68.0 %, respectively. A network meta-analysis was performed. Sphincterotomy alone and sphincterotomy with leak-bridging stenting were most commonly investigated in the included studies (see Fig. 1s in online-only Supplementary material). No significant differences were found between the five treatment modalities. Compared with sphincterotomy alone, the combination of sphincterotomy with leak-bridging stenting increased the success rate by 15 %, although this difference was not statistically significant (RR 1.15, 95 %CI 0.97 – 1.50) ([Fig. 3]). Stenting alone (either with leak-bridging or short stents) also showed a higher success rate (RR 1.10, 95 %CI 0.84 – 1.44; and RR 1.07, 95 %CI 0.72 – 1.40, respectively), compared with sphincterotomy alone. This was not the case for the combination of sphincterotomy with short stenting, where a lower success rate was found (RR 0.94, 95 %CI 0.49 – 1.29). The plots of treatment rank probabilities also showed that the combination of sphincterotomy with leak-bridging stenting had the highest probability of being the best treatment, followed by stenting alone with leak-bridging stents ([Fig. 4]).

Four studies reported data on time to leak closure [23] [24] [29] [32]. The median time to leak closure in the sphincterotomy alone, stenting (leak-bridging and short stents), and combination (with leak-bridging and short stents) groups were 3.8, 3.9, 4.7, 3.1, and 4.5 days, respectively. There was no statistical difference between the effect differences (see Table 1s in online-only Supplementary material).

Only one trial reported duration of hospital stay [24]. Mean hospital stay for sphincterotomy alone and combination therapy with leak-bridging stenting was 3 and 4 days, respectively.

All but one study [24] reported data concerning mortality. Only one death was reported in the (short) stenting group of patients after liver transplantation. The death was not related to the endoscopic intervention (graft dysfunction) [25]. All but one study [24] reported morbidity. However, only six studies reported morbidity data separately for the different intervention groups. There were 0/20 complications in the sphincterotomy alone group compared with 7/80 (8.8 %), 2/35 (5.7 %), 1/65 (1.5 %), and 0/6 in the stenting alone (leak-bridging and short) and combination (with leak-bridging and short stents) groups, respectively, without statistically significant risk differences (Table 2s). All complications were pancreatitis.

Small-diameter stents vs. large-diameter stents

Eight studies were found for this comparison [16] [23] [25] [27] [29] [30] [31] [32]. Stents with diameter < 10 Fr were considered small-diameter stents and stents ≥ 10 Fr were considered large-diameter stents. For this analysis, the results of stenting alone and combination therapy were taken together.

All of the included studies reported clinical success: 186/195 participants (95.4 %) in the small-diameter stent group and 133/136 participants (97.8 %) in the large-diameter stent group were treated successfully. There was a nonsignificant lower risk of failure in the large-diameter stent group (OR 0.47, 95 %CI 0.12 – 1.75) (Table 3s).

Only three studies reported time to leak closure [23] [29] [32]. The mean time to leak closure in the small- and large-diameter stent groups was 4.0 and 4.5 days, respectively.

There was only one death reported, which was in the small-diameter stent group after liver transplantation [25]. All studies reported morbidity, but only six studies showed the morbidity data in the different intervention groups. There were 4/119 complications (3.4 %) in the small-diameter stent group compared with 7/88 (8.0 %) in the large-diameter stent group.

Refractory biliary leaks

Only one study dealt with refractory biliary leaks after cholecystectomy. The clinical effectiveness of FCSEMS was compared with the placement of MPS [28]. There was a significantly lower risk of failure in the FCSEMS group (success rate of 100 % vs. 65 % in the MPS group). Furthermore, in successful cases, the median time to leak closure was 11 days with MPS compared with 3.5 days in the FCSEMS group. No mortality was reported. There were 0/20 complications in the MPS group compared with 2/20 (mild pancreatitis) in the FCSEMS group.

Low grade vs. high grade leaks

Four studies described leak severity. No general results could be inferred regarding the outcome measures. In one study, there was a consistent approach depending on whether the leak was low grade or high grade: sphincterotomy alone for the former (success rate 91 %) and stenting after sphincterotomy for the latter (96 %) [27]. Katsinelos et al. were only able to make a statement about low grade leaks, as only 21 % of the leaks were high grade [16]. In refractory biliary leaks, a high grade leak proved to be a statistically significant predictor of treatment failure with MPS [28]. Finally, Chandra et al. (published abstract) did not mention outcome measures regarding leak severity [24].

NBD

Only two studies reported NBD [25] [32]. The groups with NBD included only 17 and 5 patients, respectively. The clinical success was 95.5 % (21/22 patients). The time to leak closure was not reported. No mortality or morbidity was encountered.

Discussion

The first-line treatment for biliary leaks, which are mostly caused by (laparoscopic) cholecystectomy, is ERCP where different endoscopic techniques can be used. As far as we know, we performed the first systematic review with meta-analysis to investigate the optimal endoscopic approach.

The most commonly used treatment techniques are sphincterotomy, stenting, or a combination of both techniques. The reported success rate of all these interventions is very high (> 90 %) without statistically significant differences between them. However, as the combination of sphincterotomy with leak-bridging stenting and stenting alone with leak-bridging stents had the highest probabilities of being the best treatments, our results suggest a reduced risk of failure with stenting when the leak can be bridged. It should, however, be mentioned that only four studies involving small patient numbers reported on stent length and that two of these studies were prone to bias. Where possible, a leak-bridging stent was inserted, whereas in patients with leaks that were located too peripherally, a short stent was used (confounding by indication) [16] [26].

The combination of sphincterotomy and stenting seemed only preferred when the leak could be bridged. Whether or not the placement of a leak-bridging stent should be combined with sphincterotomy needs to be evaluated on a case-by-case basis (e. g. risk of pancreatitis or bleeding). When considered safe, the combination seems to be the best choice. If the leak cannot be bridged, stenting alone with a short stent may be the preferred option, as sphincterotomy alone or systematically combining the short stent with a sphincterotomy does not seem to improve the success rate. Furthermore, sphincterotomy-related complications can increase morbidity [34]. In our systematic review, however, most complications occurred, surprisingly, in the stenting groups. These results are likely to be biased by the fact that intervention-specific morbidity data were underreported for sphincterotomy (data from 20 procedures) and combination treatments (data from 71 procedures) compared with stenting alone (data from 115 procedures).

Only four studies reported on the time to leak closure. There were no significant differences between sphincterotomy, stenting, and a combination of both techniques. However, the calculated median value, even though not significantly different, was almost 1 day shorter in the combination group with leak-bridging stenting compared with any other intervention. A longer closure time is likely to lead to prolonged hospital stay, which in turn is associated with higher costs. Therefore, we cannot rule out that combination therapy is more cost-effective than stenting alone.

Comparison of small- and large-diameter stents showed no significant difference in clinical success. The vast majority of patients included in this comparison suffered from minor biliary tract injuries, and therefore generalizability to the treatment of major biliary leaks cannot be confirmed.

Although MPS can be used at a lower cost in refractory biliary leaks, a significantly lower risk of failure was reported in the FCSEMS group. Even when only successful cases were taken into account, a clearly shorter time to leak closure was observed in the FCSEMS group [28].

Directing therapy toward leak severity showed good results [27]. Our included studies, however, included insufficient data to give clear advice regarding the optimal approach in low or high grade leaks. Complex injuries, such as transection, should generally be managed surgically.

NBD was only reported in two small studies, making it impossible to draw conclusions on the appropriateness of this technique. In our opinion, NBD should be limited to patients with important co-morbidities and/or coagulopathy to avoid a second endoscopic procedure (e. g. for stent removal) or sphincterotomy.

The 11 included studies had important heterogeneity concerning study design, setting, and endoscopic interventions. We included both randomized clinical trials and observational studies, as the advantages of including both study designs in a meta-analysis, for example on generalizability of the results, may outweigh the disadvantage of basing results on only four randomized trials [35]. Overall quality of the evidence must be considered as moderate (e. g. the abovementioned possible biases and randomized trials without blinding or power analysis, possibly causing type II error). Our recommendations must therefore be interpreted with caution. As the reported success rates were very high and not all studies were (pre-registered) clinical trials, publication bias is possible. Our network approach made it impossible to draw a funnel plot, but a great advantage is that it made comparisons possible between endoscopic procedures that were not directly compared within the same publication.

In terms of future trials, we believe that large-scale randomized clinical trials are needed to further define the optimal first-line approach in patients with low grade, high grade, or refractory biliary leaks.

In conclusion, we reported high clinical success in treating biliary leaks with sphincterotomy, stenting, or a combination of both techniques, without statistical differences. The available evidence suggests a reduced risk of failure with stenting, especially when the biliary leak can be bridged. In this case, when regarded safe, the combination of leak-bridging stenting with sphincterotomy should be considered. If leak bridging is not possible, stenting alone with a short stent may be preferred. In refractory biliary leaks, the temporary placement of an FCSEMS seems to be a good option with a high success rate. An algorithm for the endoscopic management of biliary leaks is proposed in [Fig. 5].

Competing interests

None

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Corresponding author

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• Supplementary Material