Abstract
-
Background/Aims
- Walled-off necrosis (WON) is a severe complication of acute pancreatitis in children, with limited evidence on its endoscopic management. This study evaluated the efficacy and safety of endoscopic ultrasonography (EUS)-guided lumen-apposing metal stent (LAMS) placement for WON in pediatric patients.
-
Methods
- This open-label prospective study included pediatric patients aged 5–18 years with WON secondary to acute necrotizing pancreatitis that was managed with EUS-guided LAMS at a tertiary center from January 2021 to July 2023. Clinical success, defined as symptom resolution and WON clearance at 12 weeks, was the primary outcome. Secondary outcomes included technical success, complications, and the need for additional interventions.
-
Results
- Eleven patients (mean age, 15.5±3.1 years) were included. Clinical success was achieved in 90.9% of the patients within 12 weeks, with a 100% technical success rate. Two patients experienced stent occlusions that were managed with saline irrigation; one case required video-assisted retroperitoneal debridement. The mean hospital stay was 5.4±3.3 days. No major adverse events were reported.
-
Conclusions
- EUS-guided LAMS placement is a safe and effective alternative to surgery for pediatric WON, with high clinical and technical success rates and minimal complications. Further multicenter studies are required to validate these findings.
-
Keywords: Child; Endoscopy; Endosonography; Pancreatic pseudocyst; Pancreatitis; Pediatrics
Graphical abstract
INTRODUCTION
Acute pancreatitis (AP) is a pathological condition involving pancreatic inflammation. It has traditionally been considered a rare disease in the pediatric age group.1 However, according to recent data, the incidence of AP is approximately 3 to 13 cases per 100,000 persons per year.2,3 The incidence of AP is increasing worldwide, which may be due to a growing awareness of the disease, better diagnostic availability, and overall advancement of medical science. However, a higher index of suspicion is required to diagnose this condition.3 Children usually have a single episode; however, some might experience multiple episodes leading to clinical conditions such as recurrent AP and chronic pancreatitis, which can significantly impact the quality of life due to chronic pain, frequent hospitalizations, and/or nutritional deficiencies. This can hinder the growth and development of children.4
Biliary etiologies are the most common causes of AP in children, accounting for up to 30% of cases across various studies.5 Medications, such as antiepileptics, anti-cancer drugs, and immunomodulators, are the second leading cause, accounting for up to one-fourth of cases.6 Developmental anomalies are also important causes of AP and account for 20% of cases, with increasing numbers of cases being identified.7 Genetic causes, such as PRSS1, SPINK1, and CPA1 mutations, are responsible for <10% of cases of AP but contribute to >50% of cases of recurrent AP.8
The presentation of AP in young children is mostly nonspecific, and abdominal discomfort and irritability are the most common symptoms.9 AP in the pediatric population is diagnosed using the international study group of pediatric pancreatitis: in search for a CuRE (INSPIRE) criteria, which define AP as the presence of two the following: (1) abdominal pain consistent with AP, (2) serum amylase or lipase levels greater than three times the upper normal limit, and (3) imaging characteristics consistent with AP.10 Although most children have mild disease with a full recovery as the outcome, a substantial proportion require intensive care for transient organ dysfunction and develop local and systemic complications such as pancreatic pseudocyst, walled-off necrotic collection (WON), splenic artery aneurysm, acute respiratory distress syndrome, and acute kidney injury.11
WON is a critical complication of pancreatitis that is characterized by a well-defined encapsulated area of pancreatic or extrapancreatic necrosis. The management of WON in the pediatric population presents unique challenges owing to the anatomical and physiological differences between adults and children and the rarity of the condition in the pediatric population, which limits direct clinical experience and research data.12
Interventional endoscopic ultrasonography (EUS) is an evolving field for both diagnostic and therapeutic interventions. It has become the first-line treatment for the management of AP complications, such as pancreatic pseudocysts and WON in the adult population. However, similar data in the pediatric age group are lacking. Despite the demonstrated success of lumen-apposing metal stents (LAMS) in adults, their application in the pediatric population is less documented, with only a few case reports and case series published, mostly on pancreatic pseudocysts. Therefore, surgical intervention remains the mainstay for managing WON in most parts of the world.13
Previous studies have shown evidence supporting the use of EUS-guided drainage to manage local complications of AP.14-18 However, most of these reports have been from high-volume centers in the Western world. Concrete evidence warranting a place in clinical guidelines, particularly pertaining to the management of WON, is still lacking. Therefore, the current study aimed to determine the efficacy and outcomes of using EUS-guided LAMS as a primary treatment modality for the management of WON in pediatric patients with acute necrotizing pancreatitis.
METHODS
Study design and setting
This was an open-label prospective study conducted at an academic institution in northern India from January 2021 to July 2023. Data were systematically collected and analyzed by personnel blinded to the study.
Study participants
The study population included pediatric patients, aged 5 to 18 years, with a body weight of >15 kg, who had been diagnosed with severe acute necrotizing pancreatitis in accordance with the INSPIRE criteria.10 Only patients who had undergone endoscopic intervention using transgastric LAMS as the primary treatment modality for WON were enrolled in the study, after obtaining consent from the patient and guardian. Patients aged >18 years and those undergoing primary interventions other than LAMS were excluded from the study. Patients with a preexisting diagnosis of chronic pancreatitis or acute interstitial pancreatitis or those presenting with a pancreatic pseudocyst were also excluded. Additionally, patients with WON containing a >40% solid component, paracolic gutter extension of WON, uncorrected coagulopathy at the time of the procedure, or who were deemed unfit to undergo general anesthesia as per the anesthetist (blinded from the study) were excluded.
Study outline/flow
After obtaining informed consent from their guardians, participants satisfying the inclusion and exclusion criteria were enrolled in the study. Baseline demographic information (age, sex, weight, etiology and duration of AP, and comorbidities); clinical characteristics (presenting symptoms and their duration and severity of illness, per the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition (NASPGHAN) Pancreas Committee 2016 criteria); location, size and necrotic component of the WON; and laboratory parameters were collected.18
Imaging assessment
All imaging studies were reviewed by an independent radiologist who was blinded to clinical outcomes. The size of the necrotic collection was measured, and the presence of gas or debris was noted. The degree of necrosis was assessed by the endoscopist performing the procedure and an additional endoscopist (using the EUS images) who was blinded to the study. The average of all three values was used as the final degree of necrosis.
Procedural details
The LAMS (EGIS S-PD Stent; S&G Biotech) used in this study was a nitinol, braided, flexible saddle-shaped stent, which was fully covered with a silicone membrane.19 This fully covered, silicone-coated stent had double flanges to secure the stomach wall in alignment with the WON (Supplementary Figs. 1, 2, Supplementary Table 1). A 10 Fr catheter with a 16 mm body diameter and length of either 20 or 30 mm was used for delivery, and a 0.035-inch guidewire was required for deployment.
Experienced endoscopists performed the procedure under general anesthesia using a therapeutic echoendoscope (Pentax EG3870UTK; Pentax). Broad-spectrum antibiotics were administered to minimize the risk of secondary infections. The optimal cyst puncture site (transgastric) was identified using EUS with Doppler imaging, excluding the interposed vessels. A 19-gauge Cook Medical needle was initially used to puncture the WON, allowing for cyst fluid aspiration and visual inspection. A 0.025-inch guidewire was inserted into the cyst under fluoroscopic guidance, followed by tract creation using a 6 Fr cystotome. An 8 mm balloon (Hurricane; Boston Scientific) was used to dilate the tract before advancing the LAMS delivery catheter over the guidewire and into the cyst cavity.
Under EUS and endoscopic guidance, the distal and proximal flanges were deployed sequentially with the stent positioned against the WON wall. The suction function of the endoscope was used to aspirate the necrotic material after deployment. In cases of LAMS placement failure, alternative treatments were determined by the endoscopist and treating physician team. Empirical antibiotics were adjusted based on the culture sensitivity results, following institutional guidelines.
Outcomes
The primary outcome was clinical success, which was determined by the resolution of WON, assessed using ultrasonography at week 12, and the clinical improvement, defined by the resolution of the presenting symptoms. Patients who required additional endoscopic procedures before LAMS removal were included. Secondary outcomes were the technical success (defined as the precise deployment of the stent at both ends, with observed drainage of the contents), procedural time, need for additional interventions other than endoscopy, complication rates, length of hospital stay, need for intensive care unit (ICU) care, and mortality.
Follow-up
The patients were assessed on all hospitalization days. Patients who did not improve clinically within five days after LAMS insertion underwent additional procedures, at the discretion of the investigator. Saline irrigation was performed in cases of stent occlusion or clogging. Direct endoscopic necrosectomy (DEN) was planned if the patient failed to respond to saline irrigation, with a periodicity of one treatment every 2 to 5 days, depending on the decision of the investigator and the clinical response of the patient. Those who failed to respond to saline irrigation or DEN underwent percutaneous drain placement and/or video-assisted retroperitoneal debridement (VARD). Following discharge, patients with LAMS were followed up by the treating physician at biweekly intervals until 4 weeks after LAMS removal. Subsequently, they were followed up every 4 weeks for a minimum of 48 weeks. Any complications were recorded and treated accordingly. Any instances of death during follow-up were recorded and analyzed in detail, to rule out other factors. Ultrasonography was performed at 6-week intervals for the first 12 weeks and at the discretion of the treating physician thereafter. Cross-sectional imaging was avoided as much as possible, to reduce the radiation exposure.
Data sources and measurement
Data were collected using a standardized form designed to capture comprehensive clinical information. The form was piloted and revised based on the feedback, before full-scale data extraction. Two independent researchers collected the data, to ensure accuracy and completeness. Discrepancies were resolved through discussion or consultation with a third reviewer who was blinded to the study.
Statistical methods
Continuous variables were analyzed using either means with standard deviations (SDs) or medians with interquartile ranges, based on the distribution characteristics of the dataset. Categorical variables were summarized as frequencies and percentages. Continuous variables were compared using the Student t-test or Mann-Whitney U-test, depending on whether the data followed a normal distribution.
Ethical statement
Dayanand Medical College and Hospital's (DMCH) Institutional Research Board approval (Institutional Ethical Committee [IEC] approval number: DMCH/IEC/325).
RESULTS
Eleven patients who met the inclusion and exclusion criteria were included in the analysis. Of these, 7 (63.6%) were male and 4 (36.4%) were female. The mean age of the cohort was 15.5±3.1 years, with a median age of 16 years (Table 1, Fig. 1).
Baseline characteristics
The etiology of the pancreatitis was biliary in four cases (36.4%), drug-induced (valproate) in one case (9.1%), hypercalcemia (parathyroid adenoma-related) in one case (9.1%), and idiopathic in five cases (45.5%). In terms of severity, according to the NASPGHAN Pancreas Committee 2016, 10 cases (90.9%) were classified as moderately severe and 1 case (9.1%) as severe.18 The predominant presentation included fever with leukocytosis in six patients (54.5%), abdominal pain in three patients (27.3%), and vomiting in two patients (18.2%).
Laboratory and clinical parameters
The mean hemoglobin level was 11.7±1.2 g/dL, and the mean total leukocyte count was 10.8±4.7×10³/µL. Mean C-reactive protein and procalcitonin levels were 177.1±187.4 mg/L and 0.5±0.6 ng/mL, respectively. Similarly, mean serum creatinine, urea, and albumin levels were 0.6±0.2 mg/L, 21.5±3.7 mg/dL, and 3.6±0.7 g/dL, respectively. Pleural effusion was present in two cases (18.2%). Respiratory rates ranged from 14 to 24 breaths per minute (mean±SD, 18.1±3.8), pulse rates from 88 to 126 beats per minute (mean±SD, 99.5±11.0), and systolic blood pressures from 90 to 122 mmHg (mean±SD, 108.5±11.3), and the mean PaO2/FiO2 ratio was 366.4±73.4.
WON characteristics and procedural details
The mean WON diameter was 12.3±4.2 cm. The mean duration of pancreatitis at the time of LAMS insertion was 49.5±27.1 days (median, 40 days) (Table 2, Figs 2, 3). The mean percentage of solid component of the necrosis was 27%±7%. The most common locations of WON were the pancreas and peripancreas (54.5%), followed by the peripancreas (27.3%), pancreatic head (9.1%), and pancreatic body (9.1%). A transgastric approach was used for LAMS placement in all patients.
Outcomes
Patients were usually discharged 5 to 6 days post-LAMS insertion and were followed up for 48 weeks. The LAMS was removed at the end of 4 weeks in all patients. Nine of eleven patients did not require additional procedures.
Two patients experienced stent occlusion, as evidenced by worsening or persistent symptoms during the first week after LAMS insertion (Table 3). Saline irrigation was performed in both cases. One patient improved. However, the other did not respond and, in view of being in critical condition, underwent VARD. No other LAMS-related adverse events were observed. The primary outcome of WON drainage at 12 weeks was achieved in 10 (90.9%) patients. Furthermore, one patient required ICU admission because of clinical deterioration due to stent occlusion, despite saline irrigation. Consequently, this patient underwent VARD for further management. Following LAMS blockage, the patient developed respiratory failure, necessitating noninvasive ventilatory support. ICU care was initiated to ensure close monitoring and optimal management of the respiratory failure. Additionally, ICU care was continued post-VARD surgery to monitor for potential complications and provide comprehensive supportive care. The decision for ICU admission and management was made at the discretion of the treating physician who was blinded to the study, which ensured an unbiased clinical judgment.
DISCUSSION
This single-center prospective cohort study presented a comprehensive analysis of pediatric patients with WON who underwent endoscopic intervention with LAMS. The study included 11 patients aged 5 to 18 years, with a mean age of 15.5±3.1 years. The primary outcome, i.e. clinical success at 12 weeks, was achieved in 10 of the 11 patients (90.9%), whereas the technical success rate was 100%. Stent occlusion, which was diagnosed after a patient failed to improve clinically within one week following LAMS insertion, was observed in two cases that were managed with saline irrigation. No other major adverse events, such as bleeding or stent migration, were observed after LAMS insertion in any patient. No mortalities were observed in the study cohort.
Over the past few decades, advancements in science have resulted in significant advances in the management of pancreatitis and its complications. However, data on the management of WON using LAMS in the pediatric population are lacking. Moreover, the American Society of Gastrointestinal Endoscopy has recently proposed guidelines about the management of pancreatic fluid collection in the pediatric population, but the usage of LAMS as a treatment modality in this population is not advocated due to the scarcity of data.20 Moreover, the NASPHGAN pancreas committee recommended unanimously that the use of EUS-guided LAMS for the treatment of WON should be limited due to the paucity of data and may be determined on a case-by-case basis.18 Currently, the management of AP in pediatric patients is based upon the evidence in adult patients. However, EUS-guided LAMS drainage for WON in the adult population cannot be extrapolated to the pediatric population due to limited endoscopic expertise and a lack of dedicated endoscopic accessories.
After a thorough literature review, only a few cases have been reported, the details of which are summarized in Table 4.21-23 Kim and Trevino21 drained the WON in a 12-year-old boy using an EUS-guided AXIOS stent. The patient required two additional necrosectomy treatments and experienced stent migration as an adverse effect. In contrast, Ramesh et al.22 drained a WON with a double pigtail stent, and the patient required two additional endoscopic treatments. Similarly, Trevino et al.23 reported the drainage of a WON using a double pigtail stent. The authors reported clinical success without the need for additional endoscopic treatments or complications.
Compared with other studies, our study demonstrated superior outcomes in several respects. Trindade et al.24 and Giefer and Balmadrid et al.25 reported successful resolution of WONs and pancreatic pseudocysts using AXIOS stents in pediatric patients, with minimal complications. However, these studies were limited to single case reports, whereas our study provided a larger sample size and broader scope of data.
To the best of our knowledge, the current study is the first prospective and largest worldwide study on the use of LAMS for WON management in a pediatric population. The current study only enrolled patients with WON, contrary to previous studies that aggregated all types of pancreatic fluid collection, which potentially skewed the efficacy results due to the higher liquid content and naturally better outcomes associated with pancreatic pseudocysts.
Moreover, in our study, we performed on-site drainage (800–1,500 mL) during LAMS placement, which is a possible reason for the high clinical success that limits the need for additional endoscopic interventions or DEN. Therefore, we propose that LAMS insertion should be accompanied by on-site drainage to achieve better outcomes. Additionally, the use of targeted antibiotics based on fluid aspirate cultures significantly improved the resolution of sepsis. Other factors contributing to better drainage in our study included the selection of the most dependent position for drainage, precise puncture site (i.e., proximity to the gastrointestinal lumen), and precise deployment of the LAMS stent (i.e., oblique rather than horizontal) because of the holistic implementation of endoscopic, fluoroscopic, and EUS guidance, which rendered the procedure completely safe. The strength of our study lies in its successful management of large WONs, resulting in superior clinical efficacy, fewer complications, and shorter hospital stays. These factors, along with the type of stent used (i.e., not electrocautery-enabled), reduced the financial burden on the patients.
Our study had some limitations. First, we did not use a control group to compare the efficacy of LAMS with other endoscopic interventions. In addition, we restricted the maximum amount of the solid necrotic component. Therefore, the efficacy of LAMS in patients with a high degree of solid components is unclear. Furthermore, our study relied on transabdominal ultrasonography as the primary imaging modality for follow-up, owing to its lower sensitivity in detecting small residual WON compared with cross-sectional imaging techniques. Although ultrasonography was chosen to minimize the radiation exposure, particularly in the pediatric population, this approach may have led to underdetection of minor residual collections. Cross-sectional imaging was employed only when clinically indicated to balance the diagnostic precision with the radiation-associated risks.
However, our study paves the way for prospective randomized controlled trials to further validate these findings. Thus, although our study marks an initial step in advocating LAMS as the primary treatment for WON, further validation is necessary.
In summary, this study presents robust evidence supporting the use of LAMS in pediatric patients with WON, demonstrating its high technical and clinical efficacy, minimal complications, and reduced need for additional interventions. These findings suggest that LAMS is a superior and safer alternative to traditional surgical approaches and other stenting methods and offers significant benefits to pediatric patients with severe acute necrotizing pancreatitis. Further multicenter trials are warranted to confirm these results and refine treatment strategies.
Supplementary Material
Supplementary Fig. 2. The flowchart depicting procedural details of lumen-apposing metal stent (LAMS) insertion for walled-off necrosis drainage.
ce-2024-315-Supplementary-Fig-2.pdf
Supplementary materials related to this article can be found online at https://doi.org/10.5946/ce.2024.315.
Conflicts of Interest
The authors have no potential conflicts of interest.
Funding
None.
Author Contributions
Conceptualization: VM, MKG, AA, YKG, AS; Data curation: VM, MKG, AA, YKG; Formal analysis: VM, MKG, AA, YKG; Funding acquisition: VM; Investigation: VM, MKG, YK; Methodology: VM, MKG; Project administration: VM, MKG; Software: VM; Resources: VM; Supervision: VM, MKG, AS; Validation: VM, MKG, AS; Visualization: VM, MKG, YKG, AS; Writing–original draft: VM, MKG, AA, YKG, AS; Writing–review & editing: all authors.
Fig. 1.A flowchart of the study. A total of 11 patients were enrolled; 9 required no additional endoscopic interventions, and the primary outcome was achieved in 10 patients. VARD, video-assisted retroperitoneal debridement.
Fig. 2.Magnetic resonance imaging (MRI) of pediatric patients with walled-off necrosis (WON). Axial T2-weighted MRI images of four pediatric patients demonstrate large, well-encapsulated WON marked by black asterisks (*). (A) A heterogeneous fluid collection with internal debris located in the pancreatic and peripancreatic region. (B) A predominantly cystic WON located in the lesser sac, exerting mass effect on adjacent structures. (C) A large encapsulated collection with a fluid-debris level occupying most of the upper abdomen, displacing the stomach and bowel loops. (D) A clearly demarcated fluid collection with minimal internal debris located near the pancreatic tail.
Fig. 3.(A, B) Endoscopic images depict lumen-apposing metal stent draining solid necrotic debris (marked with *). (C, D) Endoscopic ultrasound images depict walled-off necrosis (WON) (I is the necrotic debris, and II depicts the liquid component) and the endoscopic ultrasonography needle in the WON cavity.
Table 1.Baseline characteristics distribution
|
Characteristic |
Value |
|
Age (yr) |
15.5±3.1 |
|
Sex (female:male) |
4 (36.4):7 (63.6) |
|
Etiology |
|
|
Biliary |
4 (36.4) |
|
Drug-induced |
1 (9.1) |
|
Hypercalcemia |
1 (9.1) |
|
Idiopathic |
5 (45.5) |
|
Severity (NASPGHAN Pancreas Committee 2016) |
|
|
Moderately severe |
10 (90.9) |
|
Severe |
1 (9.1) |
|
Predominant symptom |
|
|
Fever with leucocytosis |
6 (54.5) |
|
Pain abdomen |
3 (27.3) |
|
Vomitings |
2 (18.2) |
|
Lab investigations |
|
|
Hemoglobin (g/L) |
116.5±11.6 |
|
Total leukocyte count (×109/L) |
12.79±4.73 |
|
C-reactive protein (mg/L) |
38.59±22.31 |
|
Procalcitonin (µg/L) |
0.55±0.33 |
|
Creatinine (µmol/L) |
53.04±16.79 |
|
Urea (mmol/L) |
7.68±1.31 |
|
Albumin (g/L) |
36.1±7.4 |
|
PaO2/FiO2 ratio |
366.36±73.38 |
|
Pleural effusion |
2 (18.2) |
|
Respiratory rate (/min) |
18.09±3.75 |
|
Pulse rate (/min) |
99.45±11.03 |
|
Systolic blood pressure (mmHg) |
108.54±11.28 |
Table 2.Characteristics of walled-off pancreatic necrosis
|
Parameter |
Value |
|
Characteristics of WON |
|
|
Day of pancreatitis on which LAMS was inserted |
36.7±3.1 |
|
Mean WON diameter (cm) |
11.8±1.2 |
|
Mean solid component of necrosis (%) |
27±7 |
|
Location of WON |
|
|
Head of pancreas |
1 (9.1) |
|
Body of pancreas |
1 (9.1) |
|
Peripancreatic |
3 (27.3) |
|
Pancreatic & peripancreatic |
6 (54.5) |
Table 3.Outcome distribution
|
Outcome |
Value |
|
Primary outcome after drain of WON (week 12) |
|
|
Patients requiring no other endoscopic session |
9 (81.8) |
|
Patients requiring additional endoscopic sessions |
1 (9.1) |
|
Total |
10 (90.9) |
|
Secondary outcomes |
|
|
Technical success |
11 (100) |
|
Patients requiring additional interventions (other than endoscopic) |
1 (9.1) |
|
Procedure time (min) |
27±5.3 |
|
Complication rate (day) |
2 (9.1)a)
|
|
Length of hospital stay |
5.4±3.3 |
|
Need for ICU care |
1 (9.1) |
|
Mortality |
0 (0) |
Table 4.Previous reports on usage of lumen-apposing metal stent in pediatric patients with walled-off pancreatic necrosis
|
Study |
No. of children |
Age (yr) |
Size of collection |
Type of stent used |
Technical success (%) |
Clinical success (%) |
Complications |
Follow-up (wk) |
Additional endoscopic sessions |
|
Kim and Trevino21
|
1 |
12 |
10×4 cm |
AXIOS |
100 |
100 |
Stent migration |
12 |
2 Additional necrosectomy sessions with hydrogen peroxide |
|
Ramesh et al.22
|
1 |
8 |
Long axis diameter 12.5 cm |
10 Fr DPT |
100 |
100 |
None |
24 |
2 Additional endoscopic sessions |
|
Trevino et al.23
|
1 |
10 |
110×85 mm |
DPT |
100 |
100 |
None |
36 |
None |
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