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- Jiang Jiani1,
- Lv Fujing1,
- Chen Chuyan1 &
- …
- Jiang Wei1
BMC Gastroenterology volume24, Articlenumber:379 (2024) Cite this article
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Abstract
Background
Duodenal papillary adenoma, a potentially malignant benign tumor is primarily treated with endoscopic papillectomy. Despite its efficacy, endoscopic papillectomy has a high complication rate. This study investigates whether pancreatic duct and common bile duct stent placement can mitigate these complications.
Methods
In a retrospective observational analysis, 79 patients with duodenal papillary adenoma, treated with endoscopic papillectomy at our center, were studied. The cohort included patients who underwent endoscopic papillectomy with no stents placement, common bile duct stent placement alone, pancreatic duct stent placement alone, or stents placement in both ducts. We assessed the outcomes of endoscopic papillectomy, including complete resection rate and recurrence rate as the primary and secondary outcomes respectively. In the meantime, the incidence of complications were also analysed as the safety outcomes.
Results
Complete resection rates did not significantly differ between patients with or without stent placement (85.7% P group vs. 89.2% N-P group, P = 0.64). Early complication rates were similar across groups. However, significant reduction in common bile duct stenosis was observed in the stenting group (0% B group vs. 10.5% N-B group, P = 0.03). Furthermore, stent placement correlated with lower adenoma recurrence rates during follow-up (2.4% P group vs. 16.2% N-P group, P = 0.03; 2.4% B group vs. 15.8% N-B group, P = 0.04).
Conclusions
Pancreatic duct and common bile duct stent placement in endoscopic papillectomy may decrease late complications, particularly common bile duct stenosis, and reduce the recurrence of duodenal papillary adenoma.
Trial registration
This study received approval from the Institutional Review Board and Ethics Committee of Beijing Friendship Hospital (Approval No. BFHHZS20230203), and retrospectively registered in www.ClinicalTrials.gov (NCT06301048, Initial Release date: 02/18/2024, Last Public Release date: 03/03/2024).
Peer Review reports
Background
Ampullary tumors, with an annual incidence of approximately 0.59 per 100,000, are a significant clinical concern due to their potential for malignancy [1]. These tumors are more common in men and are primarily adenomas, benign lesions with a high risk of malignant transformation [2]. The typical age range for the onset of duodenal papillary adenoma is 40–60 years. The advancements in endoscopic techniques have not only improved the detection rates but also revolutionized the diagnostic approach, primarily relying on endoscopy and endoscopic ultrasound (EUS), with subsequent pathological examination for definitive diagnosis.
The progression of these adenomas to adenocarcinoma underscores the importance of early intervention. Endoscopic Papillectomy (EP), as a less invasive alternative to traditional pancreaticoduodenectomy, has gained prominence due to its reduced trauma and quicker recovery times [3, 4]. Pioneered by Suzuki K et al. in 1983, EP has been extensively studied over the decades, with numerous retrospective and cohort studies underscoring its safety and efficacy [5,6,7,8]. Despite its advantages, EP is associated with a broad range of complications, occurring at rates between 7.7% and 58.3% [9,10,11]. These complications can be categorized into early and late types, with early complications including bleeding, perforation, pancreatitis, and cholangitis, and late complications primarily comprising various forms of stenosis. The management of these complications often requires a balance between conservative treatment and more invasive endoscopic interventions.
In this context, the role of pancreatic duct (PD) and common bile duct (CBD) stent placement has emerged as a crucial area of investigation. These stents are proposed to not only reduce the incidence of complications following EP but also aid in hemostasis and promote wound healing. However, the application of stent placement in EP procedures remains a subject of debate, with no established consensus in the medical community. This study aims to evaluate the therapeutic outcomes and complications associated with EP, particularly focusing on the impact of PD and CBD stent placement in the management of duodenal papillary adenomas.
Methods
Study design
Our retrospective study analyzed 79 patients diagnosed with duodenal papillary adenoma at Beijing Friendship Hospital from June 2015 to March 2023. These lesions, confirmed via biopsy, were restricted to the mucosa and showed minimal (< 20mm) biliary or pancreatic duct invasion on endoscopic ultrasonography. All patients underwent endoscopic papillectomy, optionally complemented by pancreatic and biliary stent placement.
- (1)
Inclusion criteria.
- ①
Age ≥ 18 years.
- ②
Identification of duodenal papillary lesions via gastroscopy or duodenoscopy.
- ③
Intraductal involvement < 20mm.
- ④
Absence of preoperative peripheral lymph node metastasis and pancreatic/biliary duct stenosis (verified by CT, MRI, or other imaging).
- ⑤
Postoperative biopsy confirming adenoma.
- (2)
Exclusion Criteria.
- ①
Diagnosis of familial adenomatous polyposis or multiple hamartoma syndrome.
- ②
Patients undergoing pancreaticoduodenectomy within a month post-EP for residual lesions.
Research ethics
This study received approval from the Institutional Review Board and Ethics Committee of Beijing Friendship Hospital (Approval No. BFHHZS20230203), and registered in ClinicalTrials.gov (NCT06301048, Initial Release date: 02/18/2024, Last Public Release date: 03/03/2024). Because the clinical data were collected in a de-identified manner from YIDUCLOUD which is a forward-looking medical big-data platform, the requirement for consent was waived by the ethics committee.
Endoscopic procedures
Patients underwent a comprehensive preoperative evaluation, assessing general health, concurrent diseases, and specific characteristics of the lesions. Informed consent, detailing the procedure, risks, benefits, and alternatives, was obtained. Patients on antiplatelet or anticoagulant medication ceased these seven days prior to the procedure in accordance with British Society of Gastroenterology (BSG) and European Society of Gastrointestinal Endoscopy (ESGE) guidelines [12].
Endoscopic procedures, conducted by seven skilled endoscopists, utilized a range of specialized equipment, including a side-view duodenoscope, electrotomy machine, endoloop, diathermic and mucosal incision knives, and other tools for precise and safe operation. General anesthesia was administered, and patient positioning was carefully managed. Techniques like submucosal injection for lesion elevation and lesion resection were standardized. Larger lesions received tailored resection approaches.
Post-resection, endoscopic retrograde cholangiopancreatography (ERCP) was performed for stent placement as needed, with X-ray confirmation of stent positioning. There was no strict standard for stent placement, which was mainly based on the comprehensive evaluation of the scope of the lesion, intraoperative bleeding, the use of metal clips and other techniques, the exposure of the CBD duct and pancreatic duct opening after resection, and the operation time. The personal preferences of the endoscopists could also influence the choice of stent placement.
Residual lesions and hemostasis were managed using APC and metal clips. Specimens were collected for pathological analysis.
Postoperative care included fasting, administration of proton pump inhibitors (PPIs) and antimicrobials, and close monitoring for EP-related symptoms. Blood tests were conducted at set intervals post-operation. Stents were removed within 1 to 3 months, depending on individual patient requirements. Follow-ups include MRCP at six months, and gastroscopy with biopsies of the scar and any abnormal area at 3, 6, and 12 months post-operation. Adverse events were recorded as per American Society for Gastrointestinal Endoscopy (ASGE) lexicon and classification of adverse events gastrointestinal endoscopy (AGREE classification) [13].
Data records
We recorded all the following demographic, laboratory, radiography, pathological diagnosis, clinical variables, as well as endoscopic findings which include the size and feature of the lesion, procedure methods used.
Statistical analysis
All analyses were performed using the Statistical Package for Social Sciences 22.0 (SPSS22.0, IBM, Armonk, NY, United States) and Prism 9.4.1 (GraphPad, San Diego, CA, United States). The age, endoscopic maximum diameter and other measurement data conforming to normal distribution were expressed as mean ± standard deviation (x ± s), while the non-normal distribution measurement data were expressed as median (interquartile). Gender, past history, family history and other statistical data were presented as frequency (component ratio). Continuous variables with normal distribution were analyzed by group t-test. Otherwise, we used the chi-square-test. All statistical tests were conducted using two-sided tests. A p-value < 0.05 was considered to indicate statistical significance in all analyses.
Definitions
Complete resection (R0 resection) is defined as having negative pathological margins both horizontally and vertically in the resected specimens, and the absence of residual tissue confirmed by endoscopy and biopsy at a 3-month follow-up. En-bloc resection refers to the removal of the entire lesion in a single specimen [14].
Pancreatitis is diagnosed by acute typical abdominal pain with serum amylase or lippase levels more than triple the upper normal. Hyperamylasemia is indicated by increased serum amylase without abdominal pain or imaging anomalies. Cholangitis is identified by a postoperative fever of at least 38℃ lasting 24h, excluding other causes. Perforation involves evidence of air or luminal contents outside the gastric tract post-procedure [13].
Hemorrhage requires clinical intervention or transfusion, with intraoperative hemorrhage needing endoscopic or surgical management, and postoperative hemorrhage identified by symptoms like haematemesis, melena, or a significant hemoglobin drop (> 2g) within two weeks post-surgery [13].
EP-related duct stenosis is diagnosed using abdominal imaging. Lesions identified within 6 months post-surgery are classified as residual, while those found after a negative endoscopy or biopsy are considered recurrences [14].
Results
Population characteristics
The study initially enrolled 87 patients, excluding 2 and 6 patients, respectively, for familial adenomatous polyposis and post-EP surgical reasons. The study eventually recruited 79 patients, grouped based on stent placement: 26 without stents, 12 with only PD stents, 11 with only CBD stents, and 30 with both. These patients were further categorized into four groups: the Pancreatic Stenting Group (P group, n = 42), Non-Pancreatic Stenting Group (N-P group, n = 37), Biliary Stenting Group (B group, n = 41), and Non-Biliary Stenting Group (N-B group, n = 38) (Fig.1).
The study conducted comparative analyses between each stenting group and its corresponding non-stenting counterpart. No significant differences were observed in age, gender, coronary heart disease, hypertension, diabetes, antiplatelet drugs, or pathological outcomes between the groups. However, the endoscopic maximum diameter was notably larger in both the P and B groups compared to their non-stenting counterparts, with statistically significant differences (P group: 18.2 ± 8.3mm vs. N-P group: 13.9 ± 6.2mm, P = 0.01; B group: 18.5 ± 8.2mm vs. N-B group: 13.7 ± 6.3mm, P = 0.005) as shown in Table1.
Endoscopic outcomes
All patients successfully underwent EP. The use of submucosal injection and APC was more frequent in the N-P group, while endoscopic sphincterotomy (EST) and metal clips were more commonly used in the P group. Notable statistical differences were observed: submucosal injection (40.5% P group vs. 64.9% N-P group, P = 0.03), APC (4.8% P group vs. 24.3% N-P group, P = 0.01), EST (28.6% P group vs. 5.4% N-P group, P = 0.007), and metal clips (83.3% P group vs. 40.5% N-P group, P < 0.001). Additionally, biliary stents post-EP were more frequent in the P group (71.4% vs. 29.7% in N-P group, P < 0.001). The en-bloc and complete resection rates showed no significant differences between the groups (en-bloc: 95.2% P group vs. 94.6% N-P group, P = 0.90; complete resection: 85.7% P group vs. 89.2% N-P group, P = 0.64)(Table2).
In this study, the N-B group exhibited a lower frequency of submucosal injection and APC use compared to the B group. Conversely, the B group had a higher use of EST and metal clips than the N-B group, with significant statistical differences in both cases. Additionally, pancreatic stent placement post-EP was more common in the B group compared to the N-B group. Both groups showed similar rates of en-bloc resection and no significant difference in complete resection rates (Table;2). Patients with positive pathological margins underwent further endoscopic evaluations and treatments based on subsequent findings.
Clinical outcomes and complications
The hemorrhage rates, both intraoperative and postoperative, were similar between the groups, with no significant statistical differences. The incidence of post-ERCP pancreatitis (PEP), hyperamylasemia, and post-ERCP cholangitis (PEC) also showed no significant differences. There were no cases of perforation or mortality in either group. The follow-up duration varied from 8 to 36 months, with a median of 12 months. Pancreatic stents were removed between 1 and 6 months post-EP, typically at 3 months. Follow-up imaging showed no PD stenosis in either group, while CBD stenosis occurred in a few cases. Notably, the recurrence of duodenal papillary adenoma was significantly lower in the P group compared to the N-P group (2.4% P group vs. 16.2% N-P group, P = 0.03) (Table3).
No significant differences were noted in hemorrhage, PEP, hyperamylasemia, and PEC between the groups. The removal of biliary stents occurred between 1 and 7 months post-EP, typically at 3 months. Notably, the B group showed no cases of common bile duct stenosis, unlike the N-B group, which had a higher incidence (0% B group vs. 10.5% N-B group, P = 0.03). The recurrence of duodenal papillary adenoma was significantly lower in the B group (2.4% B group vs. 15.8% N-B group, P = 0.04)(Table3). Patients with intraoperative and postoperative hemorrhage were effectively treated endoscopically or medically. Those with pancreatitis and cholangitis responded well to treatment. Recurrent high-grade adenoma patient in the stenting group underwent endoscopic mucosal resection, while the non-stenting group received varied treatments, all resulting in favorable outcomes.
Discussion
Since the early 21st century, studies, including those by Desilets DJ et al., have indicated that pancreatic stent placement post-endoscopic papillectomy (EP) can reduce postoperative pancreatitis [9]. While this view is supported by some trials and systematic reviews by Harewood GC, Napoleon B, and Wang et al., which observed lower pancreatitis rates with stenting, contrasting studies by Chang WI and Kang SH et al. found no significant reduction in complications with PD stent placement [15,16,17,18,19,20,21,22]. This divergence in findings points to the need for further research to clarify the role of PD stents in EP outcomes.
In 2015, the American Society for Gastrointestinal Endoscopy (ASGE) moderately recommended PD stent placement after EP [23]. The ESGE in 2021 strongly advocated for it to reduce postoperative pancreatitis risk. They suggest pre-EP endoscopic ultrasound or MRCP to exclude pancreas divisum [24]. A 2022 Gastrointest Endosc expert consensus, backed by reviews from Spadaccini M et al. and Wang Y et al., supported PD stenting’s preventative role in EP complications, agreeing on its routine use to prevent EP-related pancreatitis [18, 25, 26]. However, a recent and extensive meta-analysis suggested that prophylactic pancreatic duct stenting did not offer a significant protective effect against post-ampullectomy pancreatitis [27]. In our study, the rate of post-ERCP pancreatitis (PEP) was slightly lower in the group with PD stent placement (P group), but the difference was not statistically significant compared to the group without stents (N-P group). Additionally, no significant correlation was found between PD stent placement and other complications post-EP. It is noteworthy that patients in the P group had larger lesion diameters, potentially leading to prolonged surgeries and larger residual scars, thus increasing the risk of hemorrhage and inflammation. On the other hand, stents were probably only placed in the highest risk patients and not placed in patients deemed to be lower risk. A 2020 study by Taglieri E et al. also suggested that increased PEP risk in the P group could be due to obscured PD openings [21].
Research on CBD stent placement after EP presents mixed findings. Studies by Ito K et al. and Lei Jiang et al. reported reduced complications, notably cholangitis, while Kang SH et al.‘s study saw no significant difference [14, 20, 28,29,30]. Guidelines from ASGE and ESGE recommend stenting in specific cases, but consensus is lacking on routine use [23, 24]. Our study aligns with the potential benefits of CBD stenting, evidenced by a marked decrease in bile duct stenosis. This may be due to the fact that bile duct stents can effectively ensure the patency of bile drainage in the short term after EP, avoiding local inflammation and edema caused by poor bile drainage. In addition, CBD stent can also support and expand the bile duct, which can resist postoperative benign stenosis caused by scar hyperplasia.
Endoscopic follow-up in our study revealed a significant difference in duodenal papillary adenoma recurrence between stenting and non-stenting groups, a finding not previously highlighted. This discrepancy could be attributed to factors like larger lesion sizes and higher pathology grades in the stenting group, leading to more extensive resections. Furthermore, some studies suggest that the occurrence of duodenal papillary adenoma may be related to pancreatic and biliary disease, which could stimulate the papilla by inflammation or stones [31]. Due to the placement of stents, adequate drainage of the pancreatic and CBD duct was ensured, consequently reducing postoperative inflammation and stenosis. Therefore, decreasing the irritation of duodenal papilla by cholangiopancreatic factors presumably be the reason for stents reducing postoperative recurrence. However, the varied follow-up duration and limited patient numbers may have influenced recurrence rates. The impact of CBD and PD stent placement on adenoma recurrence warrants further investigation through large-scale, prospective, randomized studies.
Despite some conflicting findings in literature and varying recommendations from ASGE and ESGE, our results contribute to this ongoing discussion. However, our study’s retrospective nature, limited patient numbers, and the range of follow-up periods could impact the generalizability and accuracy of our findings. Meanwhile, due to the limited sample size in this study, the grouping method we adopted may lead to the mutual interference of the effects of the two kind of stents, resulting in the bias of the results. This highlights the necessity for further large-scale, prospective, randomized studies to provide more definitive evidence and refine clinical practices in managing duodenal papillary adenoma.
Conclusions
The placement of PD and CBD stents could potentially decrease procedure-related complications, particularly those arising later, in patients undergoing endoscopic duodenal papillectomy. Additionally, stent implementation might be linked to a recurrence of adenoma. Nonetheless, to conclusively determine the effectiveness of PD and CBD stents in endoscopic papillectomy, more extensive, prospective, and randomized controlled clinical trials are required.
Data availability
Data is provided within the supplementary information files, while part of the data are not publicly available in order to protect patient privacy.
Abbreviations
- EP:
-
Endoscopic Papillectomy
- PD:
-
Pancreatic Duct
- CBD:
-
Common Bile Duct
- EUS:
-
Endoscopic Ultrasound
- BSG:
-
British Society of Gastroenterology
- ESGE:
-
European Society of Gastrointestinal Endoscopy
- ERCP:
-
Endoscopic Retrograde Cholangiopancreatography
- PPI:
-
Proton pump inhibitor
- ASGE:
-
American Society for Gastrointestinal Endoscopy
- AGREE:
-
Adverse events gastrointestinal endoscopy
- PEP:
-
Post-ERCP pancreatitis
- PEC:
-
Post-ERCP cholangitis
- ASGE:
-
American Society for Gastrointestinal Endoscopy
- ESGE:
-
European Society for Gastrointestinal Endoscopy
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We would like to thank the anonymous associate editor and the reviewers for their useful feedback that improved this paper.
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Department of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, National Clinical Research Center for Digestive Diseases, Beijing Digestive Disease Center, Beijing Key Laboratory for Precancerous Lesion of Digestive Disease, Beijing, 100050, P.R. China
Jiang Jiani,Lv Fujing,Chen Chuyan&Jiang Wei
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L.F.J., C.C.Y., J.J.N. and J.W. conceived and designed this study. J.J.N. retrieved and interpreted all data. J.J.N. and L.F.J. arbitered the results. J.J.N. performed statistical analysis. J.J.N. drafted the original manuscript. L.F.J., C.C.Y. and J.W review and edit the manuscript. All authors read and approved the final manuscript.
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This study received approval from the Institutional Review Board and Ethics Committee of Beijing Friendship Hospital (Approval No. BFHHZS20230203), and registered in www.ClinicalTrials.gov (NCT06301048). Because the clinical data were collected in a de-identified manner from YIDUCLOUD which is a forward-looking medical big-data platform, the requirement for consent was waived by the ethics committee.
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Jiang, J., Lv, F., Chen, C. et al. Effectiveness of endoscopic papillectomy with stent placement in pancreatic and bile ducts for treating duodenal papillary adenoma: a retrospective study. BMC Gastroenterol 24, 379 (2024). https://doi.org/10.1186/s12876-024-03466-7
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DOI: https://doi.org/10.1186/s12876-024-03466-7
Keywords
- Duodenal papillary adenoma
- Endoscopic duodenal papillectomy
- Stent
- Complication