|Ahead of print publication
EUS-guided choledochoduodenostomy for malignant biliary obstruction: A multicenter comparative study between plastic and metallic stents
Rodrigo Roda Rodrigues da Silva1, Marcio Roberto Facanali Junior2, Vitor Ottoboni Brunaldi3, Jose Pinhata Otoch4, Ana Carolina Aguiar Rocha5, Everson Luiz de Almeida Artifon4
1 General Surgery Department, University of São Paulo Medical School, São Paulo; Alfa Institute of Gastroenterology, HC/EBSERH, Federal University of Minas Gerais, Belo Horizonte, Brazil
2 Gastroenterology Department, University of São Paulo Medical School, São Paulo, Brazil
3 Center for Digestive Endoscopy, Surgery and Anatomy Department, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil
4 General Surgery Department, University of São Paulo Medical School, São Paulo, Brazil
5 University of São Paulo Medical School, São Paulo, Brazil
|Date of Submission||11-Oct-2021|
|Date of Acceptance||21-Jul-2022|
|Date of Web Publication||04-Oct-2022|
Vitor Ottoboni Brunaldi,
Bandeirantes Av. 3900, Ribeirão Preto City, São Paulo State
Source of Support: None, Conflict of Interest: None
Background and Objectives: EUS-guided choledochoduodenostomy (EUS-CDS) is commonly employed to address malignant biliary obstruction (MBO) after a failed ERCP. In this context, both self-expandable metallic stents (SEMSs) and double-pigtail stents (DPSs) are suitable devices. However, few data comparing the outcomes of SEMS and DPS exist. Therefore, we aimed to compare the efficacy and safety of SEMS and DPS at performing EUS-CDS. Methods: We conducted a multicenter retrospective cohort study between March 2014 and March 2019. Patients diagnosed with MBO were considered eligible after at least one failed ERCP attempt. Clinical success was defined as a drop of direct bilirubin levels ≥ 50% at 7 and 30 postprocedural days. Adverse events (AEs) were categorized as early (≤7 days) or late (>7 days). The severity of AEs was graded as mild, moderate, or severe. Results: Forty patients were included, 24 in the SEMS group and 16 in the DPS group. Demographic data were similar between the groups. Technical success rates and clinical success rates at 7 and 30 days were similar between the groups. Similarly, we found no statistical difference in the incidence of early or late AEs. However, there were two severe AEs (intracavitary migration) in the DPS group and none in the SEMS cohort. Finally, there was no difference in median survival (DPS 117 days vs. SEMS 217 days; P = 0.99). Conclusion: EUS-guided CDS is an excellent alternative to achieve biliary drainage after a failed ERCP for MBO. There is no significant difference regarding the effectiveness and safety of SEMS and DPS in this context.
Keywords: biliary drainage, EUS, endoscopic, jaundice, stent
|How to cite this URL:|
da Silva RR, Facanali Junior MR, Brunaldi VO, Otoch JP, Rocha AC, Artifon EL. EUS-guided choledochoduodenostomy for malignant biliary obstruction: A multicenter comparative study between plastic and metallic stents. Endosc Ultrasound [Epub ahead of print] [cited 2022 Nov 28]. Available from: http://www.eusjournal.com/preprintarticle.asp?id=357879
| Introduction|| |
Endoscopic biliary stenting by ERCP is the gold standard palliative treatment for jaundice due to malignant biliary obstruction (MBO). It carries clinical success rates of around 90% of cases. However, if the ERCP fails, several options arise, and the treatment of choice is not consensual. Percutaneous transhepatic biliary drainage (PTBD), surgical, re-do ERCP, or EUS-guided BD (EUS-BD) are the main alternatives in this setting.
Although the EUS-BD is the most recent among those modalities, it has gained broad acceptance and is already considered the best alternative in referral centers., This is because EUS-BD has high technical and clinical success rates and low adverse event rates (AEs), and it is less invasive as all drains are internal. Moreover, experts can perform immediately after a failed ERCP, avoiding an extra procedure.,
Hepatogastrostomy, antegrade drainage, and EUS-guided choledochoduodenostomy (EUS-CDS) are the main EUS-BD types. Although there is no consensual access route to address distal MBO, the EUS-CDS is usually the preferred one since it is easier to perform, it foregoes dilation of the liver parenchyma, and it is not contraindicated by ascites., Furthermore, comparative studies suggest that EUS-CDS carries a lower AE rate than the other routes.,
Both self-expandable metallic stents (SEMSs) and double-pigtail stents (DPSs) have been employed to perform the EUS-CDS.,, Although SEMSs could hypothetically lead to better BD due to their larger diameter, only a few small sample size, heterogeneous articles are currently available.,, Therefore, we designed this multicenter cohort study to compare the outcomes of SEMS and DPS in performing EUS-CDS for distal MBO.
| Methods|| |
Study design and ethics approval
This was a multicenter retrospective cohort study conducted from March 2014 to March 2019 in three Brazilian tertiary referral centers (Hospital das Clínicas da Faculdade de Medicina da USP, Hospital Ana Costa de Santos, and Hospital da Clínicas da Universidade Federal de Minas Gerais). It was approved by the Internal Review Board (IRB) of the University of São Paulo Medical School, the coordinating center (registry number 33401614.0.0000.0068). Later, it was submitted and approved by the other participating centers' IRBs.
The inclusion criteria were as follows:
- Age ≥18 years
- Clinical and laboratory diagnosis of obstructive jaundice
- Presence of periampullary neoplasms such as pancreatic, major papilla, and duodenal cancer, or distal cholangiocarcinoma requiring drainage
- Patients with any contraindication for a curative surgery
- A documented previously failed ERCP.
Patients with uncorrectable coagulopathy (international normalized ratio >1.8), severe ascites, esophageal or gastric strictures, past medical history of total or subtotal gastrectomy, or tumor invasion at the puncture site were excluded from this study. All patients signed written consent for the procedure.
Immediately before the procedure, all patients were graded according to the Eastern Cooperative Oncology Group (ECOG) and Karnofsky Performance Status criteria. All procedures were carried out in advanced endoscopy centers equipped with advanced life support materials. In addition, all institutions had onsite surgical and interventional radiology teams to manage potential complications or perform PTBD in case of technical failure.
All procedures were performed under general anesthesia, but patient positioning (prone or supine) was at discretion of the endoscopist.
A linear echoendoscope (GF-UCT-160, CV160, Olympus Corporation, USA; EG-530UT, 7000 and 8000 processors, Fujinon, Japan; or EG3870UTK, Hitachi 5500 processor, Pentax, USA) was introduced to the duodenal bulb to identify the extrahepatic common bile duct (CBD).
After assessing the transverse diameter of CBD, the endoscopist selected the best puncture site aiming to direct the needle toward the hepatic hilum. Then, the puncture was performed with a 19G fine-needle aspiration (Boston Scientific, Medi-Globe, or Cook Medical). After aspiring bile to confirm positioning, a cholangiography was obtained, followed by introducing a 0.035” hydrophilic guidewire into the intrahepatic bile ducts. Then, a 6 Fr or 10 Fr cystotome or a needle knife was used to create the fistulous tract, followed by dilation using a 6-mm hydrostatic balloon. Finally, the stents (10 Fr × 07 cm double-pigtail stents or 100 mm × 60 mm partially covered SEMS, Boston Scientific, USA) were deployed under fluoroscopic and endoscopic guidance [Figure 1]. Procedure time was measured from the puncture of the CBD until the release of the stents.
|Figure 1: Technical steps of the EUS-guided choledochoduodenostomy. (a) Puncture of the dilated bile duct with a 19G needle; (b) Cholangiography to confirm correct positioning; (c) Tract creation using a needle knife; (d) Tract dilation using an 8-mm biliary balloon; (e) Deployed metallic stent; (f) Deployed plastic stent|
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All patients received broad-spectrum antibiotics (ciprofloxacin 500 mg PO BID and metronidazole 500 mg PO TID) for 7 postprocedural days. Painkillers and proton-pump inhibitors were prescribed on a case-by-case basis.
Outcomes and definitions
The primary outcome was the clinical success rate, defined as a reduction by at least 50% in direct bilirubin levels, assessed on day 7 and day 30 postdrainage.
The secondary outcomes were technical success rate (correct positioning of the plastic or metal stents in the extrahepatic biliary tract), AE rates (early defined as arising within the 1st 7 days, and late as those after the 7th postdrainage day), overall survival (days), and procedural time (time elapsed from CBD puncture until deployment of the distal edge of the stent).
Stent misdeployment was subdivided into proximal (too proximal release, either inside the biliary tree or in the retroperitoneal cavity) and distal (too distal release, leaving the stent inside the digestive lumen but outside the bile duct). That was an immediate diagnosis. If the stent was properly deployed, but later found to be inadequately positioned, that was considered a stent migration.
Stent obstruction was defined as an association of worsening jaundice with evidence of debris or sludge inside the stent. Biliary leak was defined as contrast leaking outside the CBD at the time of stent placement. Biliary peritonitis was defined as the presence of bile in the abdomen with clinical and laboratory disorders suggesting a systemic inflammatory or infectious condition.
The severity of AEs was graded according to Cotton et al.'s proposition.
Patients were followed per protocol through office visits 7, 15, 30, 60, and 90 days after the procedure. Besides clinical evaluation, researchers also ordered laboratory tests, including liver function tests. For patients missing the scheduled visits, follow-up was carried out by phone calls. Furthermore, their medical records were reviewed to assess for complications or death.
Data were presented in frequency tables with the absolute numbers and their respective percentages and descriptive measures (means and standard deviation) for quantitative data. Quantitative variables were tested for normality using the Kolmogorov–Smirnov test. For normal distribution variables, Student's t-test was used. For comparisons between nonnormal distribution variables, the Chi-square test and the Fisher test or Monte Carlo simulation were employed. For the overall analysis, Kaplan–Meier curves were obtained and compared using the log-rank test.
We considered significant those comparisons with P < 0.05 with a power of 80%. An experienced statistician ran all analyses using the IBM SPSS Statistics for Windows, Version 20.0. (Armonk, NY, USA).
| Results|| |
From March 2014 to March 2019, 44 patients with palliative distal MBO had failed ERCPs in the participating centers. Four patients met the exclusion criteria, as follows: previous gastrectomy (1), uncontrolled coagulopathy (1), neoplastic stricture at the duodenal bulb (1), and refusal to accept EUS-BD (1). Therefore, they were removed from the study.
The remaining sample comprised 40 patients, 24 receiving SEMSs and 16 undergoing CDS with a DPS [Figure 1]. The groups presented similar mean age and gender distribution. [Table 1] summarizes the demographic data.
|Table 1: Characteristics of patients and adverse events according to the allocation group|
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All patients had jaundice at the procedure, and ten patients had clinical signs of cholangitis (3 DPSs and 7 SEMSs). In addition, three patients in the SEMS group had neoplastic strictures in the descending portion of the duodenum and received a same-session duodenal SEMS.
The technical success rate was similar in both the groups (SEMS 95.8% vs. DPS 81.2%; P = 0.28). The single technical failure in the SEMS was due to an anesthetic complication, and the patient was later referred to PTBD. Among the three cases of failure in the DPS cohort, two were also referred to PTBD. However, the remaining individual was managed conservatively with antibiotics and nil per os. During this procedure, the operator found extreme resistance to insert the DPS after puncture and tract dilation. Interestingly, the patient presented progressive improvement in bilirubin levels. Seven days after the procedure, an abdominal computed tomography (CT) showed aerobilia and no abdominal collection. At the same time, an upper endoscopy revealed a large fistulous orifice in the duodenum communicating with the CBD.
Accordingly, clinical success was equivalent between the SEMS and DPS groups at 7 and 30 days. [Table 2] outlines technical and clinical success rates.
Concerning laboratory improvement, there was no statistical difference between total bilirubin and direct bilirubin levels at 7, 30, 60, and 90 days postprocedure. [Figure 2] depicts the bilirubin levels.
|Figure 2: Boxplot illustrating the drop in total and direct bilirubin levels at 0, 7, 30, 60, and 90 days after the procedure|
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In both the groups, the drop in total and direct bilirubin levels was more abrupt in the 1st week after the procedure but continued throughout the entire follow-up period. The clinical success rate was higher at day 30 than at day 7 in both the groups (90.5% SEMS and 84.6% DPS; P = 0.68).
There were six and two early AEs in the SEMS and DPS groups, respectively (ns.). Regarding timing for AEs, there was no difference between the SEMS and DPS groups [Table 3]. Among the early AEs, two patients in the DPS group experienced stent misplacement toward the abdominal cavity immediately after deployment. In the SEMS group, no patient presented stent misplacement, but other AEs were more frequent. [Table 3] describes the early AEs according to the allocation group.
|Table 3: Types of early adverse events according to allocation and the corresponding severity according to Cotton et al.|
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Four patients experienced late AEs, all related to stent obstruction (SEMS 3 and DPS 1). SEMS obstruction cases due to food impaction were managed by biliary balloon sweeping followed by an additional plastic stent insertion. For the single DPS obstruction case, we decided to remove the stent leaving a biliary fistula with no stent. One patient in the SEMS group returned for celiac plexus neurolysis 30 days after drainage. At this time, we detected a proximal migration of the stent and a well-consolidated fistula with spontaneous BD to the duodenum. Since there was no clinical repercussion, we did not consider it an AE. Food residues were the cause of the single early obstruction in the SEMS group. Initially, we managed it through balloon sweeping followed by insertion of a plastic stent inside the metallic. After the recidivism of the obstruction, the patient was referred for PTBD. Unfortunately, after the external drainage, he presented with severe hemobilia leading to death.
In the SEMS group, five AEs were moderate and one was mild. In the DPS cohort, the two AEs were severe since they required immediate surgical treatment (intracavitary stent migration). Regarding late AEs, all stent obstructions (3 SEMSs and 2 DPSs) were moderate in severity.
The SEMS and DPS groups' median survival was 117 and 217 days, respectively (P = 0.998). At 90 days, the survival rates for the SEMS and DPS groups were 78.3% and 73.3%, respectively. At 120 days, those rates were 47.8% and 53.3%. [Figure 3] demonstrates the survival curves for both the groups.
|Figure 3: Survival curves in days according to the type of stent used; P = 0.99 (log-rank test)|
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| Discussion|| |
EUS-CDS is considered an excellent alternative to relieve jaundice in patients with neoplastic lesions of the extrahepatic biliary tract after a failed ERCP. Some randomized trials and meta-analyses have recently demonstrated that it could even be considered a primary approach if difficult biliary cannulation is anticipated., Although the technical steps for CDS are well established, which stent to use is still a controversial topic. Most experts prefer the SEMS, but it is more expensive, not always available, and not necessarily cost-effective.
This study is the largest multicenter cohort comparing the 10 Fr DPS and the partially covered SEMS specifically in EUS-CDS procedure. Our groups were homogeneous regarding age, sex, and ECOG performance status. Although selection bias is intrinsic to cohort studies, stent availability in our public hospitals, rather than any demographic or clinical characteristic, was the most relevant factor for decision-making between SEMS or DPS. This fact probably explains homogeneity between the groups, which is unusual for nonmatched cohorts.
Technical success rates were similar to those reported in the literature. Our study found no statistical difference between the groups, despite a 15% absolute difference in favor of the SEMS (95.8% vs. 81.2%; P = 0.28). However, we believe that this may represent a real difference that our study failed to demonstrate, possibly due to a small sample size. The outer diameter of the SEMS introducer sheath (8.5 Fr) is thinner than the DPS's (10 Fr), and it has a conic rather than a straight tip. Those characteristics may facilitate the introduction of the metallic stent, which might eventually translate into better technical success rates.
A case of technical failure was fascinating. After failure to introduce the DPS, the patient was managed conservatively with antibiotics and nil per os. Of note, this subject had an uneventful postprocedural course and experienced a progressive improvement in bilirubin levels. The follow-up CT revealed aerobilia and no abdominal collection, suggesting that the nonoperative management may be a plausible alternative in cases of technical failure.
As per previous literature, we assessed clinical success at 7 and 30 days after the procedure. Interestingly, four patients achieved clinical success between the 7th and 30th postprocedural days, suggesting that the 7-day usual threshold might not apply to all individuals. Other clinical and laboratory information should be considered before deeming the drainage inadequate. Patients with progressive instead of an abrupt decrease in bilirubin levels and systemic improvement are possible candidates for more prolonged observation and conservative management. Hypothetically, the difference in time to restore adequate liver function may be related to the degree of hepatocellular damage before drainage. Once the biliary obstruction is relieved, the liver gradually resumes its ability to conjugate and eliminate bilirubin, which may take more than a week.,
The incidence of early and late AEs was also similar between the groups. Regarding immediate ones, the overall rate was 22.5% (29.2% SEMS vs. 12.5% DPS; P = 0.213). Albeit those arising from DPS drainage were less frequent, they were also graded as more serious. The two cases of proximal migration were referred for emergency surgery. In both cases, subhepatic drainage and stent removal were carried out, but surgeons could not identify the CDS site.
In the DPS group, two patients had cavity-migrated stents after adequate deployment in the duodenal bulb. In this sense, the positioning of the DPS seems less controllable than the SEMS. Once the proximal tail assembles into its typical pigtail-like shape, it may pull the distal part of the stent, causing its distal edge to migrate proximally. Unfortunately, this assembly may not happen immediately, causing a good initial position to become a misplacement. Perhaps, the employment of a longer DPS could mitigate such risk as its extra length allows some mobility without leading to complete migration. Likewise, stent dislodgment would be minimized if its curved end had a smaller diameter.
Contrary to the DPS, the SEMS has radiopaque markers that facilitate the deployment. Furthermore, as long as the operator does not trespass the no-return point, it can be relocated as necessary before its definitive release. Those characteristics may explain why there is a less significant misdeployment rate related to the metallic stent.
An interesting observation is the high food impaction rate. Although less frequently described,[18–20] it occurred in four patients in our SEMS cohort. Food impaction is rare in ERCP-guided drainage due to the typical lateralized position the stent assumes after deployment. On the contrary, the stent usually stays frontal to the pylorus in a CDS, favoring the accumulation of food residues. Therefore, routine association with a DPS or the development of a valved stent could eventually mitigate the food impaction risk.
Although large-caliber stents allow for a more intense biliary flow, we found no significant difference in bilirubin decline rates of SEMS and DPS. This information suggests that the flow through a 10 Fr stent overcomes the liver capability of bile production and clearance, even after long-term obstructive jaundice. Accordingly, previous data show that a 7 Fr stent is enough to relieve biliary obstruction. Moreover, the mean diameter of a normal CBD is around 3.6 mm, which corresponds to 10 Fr, which ultimately suggests that increasing the stent diameter beyond this threshold grants no further clinical benefit.
Despite the allocation group, the short overall survival rate highlights the dismal prognosis associated with such a clinical condition. Even though a cost-effectiveness analysis is mandatory, our data advocate for the superiority of the DPS since it has an immediate lower cost. In other clinical conditions, the SEMS only becomes advantageous over plastic stents after a longer follow-up demanding numerous exchanges when the latter is employed.
More recently, the lumen-apposing metal stent has also been proposed to perform EUS-guided BD. Data show high technical and clinical success rates with an acceptable incidence of AEs. Nonetheless, the total number of patients treated with such stents remains low. Furthermore, some experts advocate that it may favor food impaction due to its shorter length, larger diameter, and typical forward-facing position toward the pylorus. Finally, although attractive because of their ease of placement, they are even more expensive than conventional metal stents.
Current guidelines recommend SEMS over DPS to perform the EUS-BD based on previous data on AEs., However, the supporting evidence is weak and heterogeneous as it pools outcomes from hepaticogastrostomy and CDS routes., Of note, one of those studies failed to demonstrate significant differences between SEMS and plastic stents regarding AEs. Thus, our study is the first head-to-head article directly comparing the outcomes of DPS and SEMS in performing CDS. As we also found no difference between stent types, this study undoubtedly provides critical evidence that may shape future updates in the current clinical guidelines.
Our results are not exempt from critics and limitations. First and foremost, this was not a randomized trial, allowing for the intrinsic selection bias. However, as mentioned above, we conducted this study mainly in Brazilian public hospitals where stent shortages are common. In this sense, stent availability was the most relevant factor in selecting patients for DPS or SEMS, mitigating the selection bias based on any clinical or demographic characteristic. This observation probably explains the homogeneity between cohorts at baseline. Second, our sample was small, which might have increased the probability of a beta error. That is the shortcoming of our highly specific inclusion criteria. As it creates more homogeneous clinical scenarios, it also hampers pooling larger samples. Still, we created direct comparative data between DPS and SEMS, which allowed a more accurate sample size calculation for a further randomized controlled clinical trial.
| Conclusion|| |
EUS-guided CDS is an excellent alternative to achieve BD after a failed ERCP for MBO. There is no significant difference regarding the effectiveness and safety of SEMS and DPS in this context. Further randomized trials and cost-effectiveness studies are necessary to confirm our results.
Financial support and sponsorship
Conflicts of interest
Everson Luiz de Almeida Artifon is an Associate Editor of the journal. This article was subject to the journal's standard procedures, with peer review handled independently of the editor and his research group.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3]