The common causes of pancreatic fluid collections (PFCs) in children worldwide are trauma, gallstone pancreatitis, hereditary, viral, or toxin-mediated, and idiopathic pancreatitis. Trauma is the leading cause in children in the United States accounting for up to 50% of cases, with a significant proportion requiring surgical intervention (1). Traditionally, conservative management is advocated for PFCs <6 cm, whereas surgical intervention is suggested for PFCs measuring 10 cm or more as a result of the risk of spontaneous rupture (2). Children with pancreatic injuries have been shown to have a nonoperative failure rate of 26% to 33%, and a surgical mortality and morbidity rate of 0% and 11%, respectively (3,4). Other nonsurgical treatment options include conservative management, percutaneous drainage, and endoscopic therapy (5,6).
Endoscopic cystenterostomy entails the creation of a fistulous tract between the PFC and the gastric (cyst-gastrostomy) or duodenal lumen (cyst-duodenostomy). After establishing access to the PFC, a nasocystic catheter or transmural stent is placed into the collection to facilitate drainage. The obvious limitation of this technique is its relatively “blind” approach. The risk of perforation is particularly high when endoscopically visible luminal compression (LC) is absent (6–8). Another major complication is hemorrhage that is encountered in approximately 6% of cases (7–11). The ideal approach for PFC drainage would be to combine endoscopy with real-time visualization of the drainage procedure using endosonography. Several authors have described the use of endoscopic ultrasound (EUS) for guidance of transmural puncture and performing drainage (12–17). Using this technique, puncture of PFC under direct sonographic visualization is possible in patients without LC and in those at high risk for bleeding, such as portal hypertension (17–19).
In the adult population, there is a recent trend in favor of EUS-guided PFC drainage (10,11). Prospective, randomized trials have conclusively proven that the technical outcomes and safety profile of EUS are superior to conventional endoscopy for transmural drainage of pancreatic pseudocyst and comparable with surgical cystogastrostomy (20–22).
Although there are several reports on the efficacy and safety of EUS in the diagnosis and management of pancreaticobiliary disorders in children (23), data on the role of EUS-guided drainage of PFCs are scant. In the present study, we report our experience with single-step EUS-guided drainage of PFCs in children.
The baseline demographics, procedural indications, technical details, and outcomes of all of the patients who underwent EUS-guided drainage of PFCs during a 5-year period (October 2007–January 2012) were recorded prospectively in an electronic database. Children younger than 18 years who underwent EUS-guided drainage of symptomatic PFCs that measured >6 cm and were treated with placement of transmural stents were included in the study. Excluded were patients who underwent only a diagnostic examination or just a cyst aspiration. Before EUS, all of the children underwent contrast-enhanced computed tomography (CT) of the abdomen at our institution, unless an outside CT was of comparable quality and performed within 1 week. Intravenous ciprofloxacin was administered before the procedure and oral ciprofloxacin 250 mg twice per day for 3 days postprocedure was standard protocol. All of the procedures were performed under general anesthesia. Before EUS, all of the patients underwent endoscopic retrograde pancreatography (ERP) to bridge any pancreatic ductal leak by transpapillary stent placement, unless gastric outlet obstruction precluded duodenoscope passage.
Following ERP, PFC drainage was performed in the same endoscopic session using a curvilinear array echoendoscope (GF-UCT 140; Olympus America, Melville, NY). At EUS, the linear array echoendocope was advanced to the duodenum and gradually withdrawn to identify the extraluminal PFC (Fig. 1A). Once the PFC was identified, a 19-gauge FNA needle (Echotip, Cook Medical Inc, Bloomington, IN) was introduced into the PFC under EUS guidance (Fig. 2A), and a sample of the aspirate was sent for Gram staining and culture. Before puncture, color Doppler was used to exclude collateral vessels in the path of the needle and only PFCs located within 1 cm of the EUS transducer were drained. A 0.035-in. guidewire was then coiled within the PFC under fluoroscopic guidance (Fig. 1B, 2B). The tract was then sequentially dilated first by passing a 4.5-F endoscopic retrograde cholangiopancreatography (ERCP) cannula (Proforma HF, Conmed Technologies, Utica, NY) and then an 8- to 15-mm balloon dilator (Fig. 1C). Following dilation, one or two 7- or 10-F double-pigtail endoprostheses were deployed (Fig. 1D, 2C). Electrocautery was not used to puncture the PFC in any patient. All of the patients were observed for 2 hours following their procedures and then transferred to inpatient rooms. Immediate complications that occurred during the procedure were documented by the endosonographer and delayed complications were assessed by a 30-day follow-up telephone call.
Parents of all of the children provided written informed consent for the procedure, and the study was approved by the University of Alabama at Birmingham institutional review board.
A repeat CT of the abdomen was obtained at 48 to 72 hours postprocedure to assess response to therapy. If the PFC had diminished in size by 50% and patients were symptomatically better, they were discharged from the hospital. In patients with a suboptimal treatment response, repeat EUS-guided drainage was undertaken. A CT scan was then obtained at 8-week outpatient follow-up. In patients with treatment success, the transmural and transpapillary stents (if present) were removed by endoscopy. In patients with treatment failure, a repeat EUS-guided drainage, surgery, or percutaneous drainage was undertaken after interdisciplinary consultation.
Technical success was defined as the successful placement of 1 or 2 endoprostheses through the cystgastrostomy fistulous tract without any complications. Treatment success was defined as a decrease in the size of the PFC to at least 2 cm on CT with complete resolution of symptoms at 8 weeks postprocedure. Treatment failure was defined as the failure of the PFC to decrease to <2 cm or an increase in PFC size with persistence of symptoms at 8 weeks postprocedure. Complications were classified as major and minor. All perforation was classified as major and was diagnosed when pneumoperitoneum was evident on imaging studies in association with peritoneal signs. All infection was classified as major and was defined as any septic event after the initial endoscopic drainage caused by contamination of the pseudocyst, proven by new-onset fever, positive blood cultures, or by fluid cultures obtained at endoscopic revision. Major bleeding was defined as any hemorrhagic event that required endotherapy, blood product transfusion, inpatient observation, or presence of dry blood within the pseudocyst or gastrointestinal lumen at autopsy. Minor bleeding was defined as self-limited bleeding that occurred during transmural drainage of the pseudocyst that resolved by itself without the need for any intervention during endoscopy. Stent migration was classified as minor complication and was defined as the need to retrieve a stent from within the pseudocyst or enteral lumen.
Procedural duration was defined as the time between endoscopic intubation and withdrawal of the echoendoscope after completion of requisite therapy. Time for ERCP was not taken into consideration while calculating procedural duration for PFC drainages.
The baseline characteristics of patients and PFCs were summarized as mean, standard deviation, median, interquartile range (IQR), and range for continuous variables such as age, white blood cell count, albumin, and PFC size. Categorical variables such as sex, race, and PFC etiology were, however, expressed as frequencies and proportions. Procedure details including procedure duration and length of hospital stay, as well as the outcome measures (technical and treatment success, complication rates), were also summarized in a similar manner. The datasets were compiled using Microsoft Excel (Microsoft, Redmond, WA) and Stata 10 (STATACorp, College Station, TX).
Patient and PFC Characteristics
Between October 2007 and January 2012, 7 children underwent EUS-guided drainage of PFCs at out institution. The mean age of the patient cohort was 8.4 years (standard deviation 2.1 years) and consisted of 4 boys (57%) and 3 girls (43%). The majority of children were of white ethnicity (n = 5; 71%), and trauma was the most common etiology accounting for 5 cases (71%). The size of PFCs ranged from 80 to 170 mm (median longest axis diameter, 120 mm). All of the PFCs were pseudocysts located either in the body or in the tail of the pancreas, with the exception of one patient who had walled-off pancreatic necrosis. The median time to intervention from inciting event was 4 weeks (IQR 2–6). The baseline patient and PFC characteristics along with procedural outcomes are shown in Table 1.
Technical and Treatment Outcomes
Before EUS-guided drainage, a pancreatogram was obtained in 4 cases (57%) and transpapillary pancreatic duct stents were deployed in 2; in 2 other patients, there was a disconnected duct syndrome. ERCP was technically not feasible in the remaining 3 patients because of gastric outlet obstruction induced by the PFCs.
EUS-guided PFC drainage was technically successful in 100% of children. At EUS, an LC was evident in only 4 children (57%) and all of the drainages were performed via the transgastric route. Microbial culture and Gram stains were negative in all of the cases. Postprocedure, 6 of 7 (85.5%) patients were symptomatically better. A follow-up CT demonstrated >50% decrease in PFC size in 5 patients; the PFC persisted in size in 2 others. Although one patient had no change in PFC size despite symptom relief, the other patient with walled-off pancreatic necrosis had one other noncommunicating PFC. Both patients underwent another session of EUS-guided drainage with placement of more transluminal stents that yielded both a symptomatic and radiological response. The median procedural duration was 12 minutes (IQR 12–20 minutes) and postprocedure hospital stay was 3 days (IQR 2–7 days).
At 8-week follow-up, the rate of treatment success was 100%. All of the patients had complete resolution of the PFC on CT imaging and were asymptomatic. The transmural and transpapillary stents were removed by endoscopy. At a median follow-up of 1033 days (IQR 193–1167 days), all of the children were doing well without PFC recurrence. No complications were encountered in these children.
The findings of the present study demonstrate that single-step EUS-guided drainage is a minimally invasive, safe, and a highly effective technique for the management of symptomatic PFCs in children. The procedure was technically feasible in children as young as 6 years and precluded the need for a surgical cystogastrostomy in all of the patients.
In a study of 10 children, Jazrawi et al (24) reported satisfactory outcomes with EUS-guided treatment for pancreatic pseudocysts; however, several patients in that study underwent only cyst aspiration and not pseudocyst drainage (Table 2); the single-step EUS-guided drainage technique was adapted in only 3 cases. Also, the median age of children in that study was 14 years and the median size of PFC was 7.8 cm. In the present study, the patients were much younger (median age 8.4 years), PFC size larger (median size 12 cm), and all of the patients were treated using the single-step technique. Of the 7 children enrolled in the present study, 1 had walled-off pancreatic necrosis that required 2 interventions for adequate drainage and symptom relief. In a recent study of 211 adult patients who underwent endoscopic drainage of PFCs, patients with walled-off pancreatic necrosis had less treatment success and required more reinterventions than patients with pancreatic pseudocysts (25). This is because the necrotic contents are more thick and prone to infection when instrumented. Therefore, a more aggressive approach is warranted in the treatment of these patients.
In the present study, LC was evident at endoscopy view in only of 4 of 7 children. All of the 3 children without an LC had a PFC located in the tail of the pancreas. Pancreatic tail collections typically do not cause LC in the stomach because they are located in the lesser sac or adjacent to the spleen/left kidney. In a prospective study, we have shown that PFCs in the tail region are an independent predictor for failure of “blind” endoscopic drainage, and EUS guidance is mandatory for safe drainage of these collections (26). In 2 randomized trials that compared EUS and gastroscopy for transmural drainage of pseudocysts, the rates of technical success were significantly better for the EUS-guided approach (20,21). Although there was no difference in the overall rates of complications between both modalities, patients randomized to gastroscopy had clinically relevant complications that included death from delayed bleeding, blood transfusion, and interventional radiology-guided coil embolization. Given these inherent advantages, EUS is presently the standard of care for drainage of PFCs in adults with recent studies showing a favorable trend toward the EUS-based treatment approach (27).
The need for concomitant transpapillary pancreatic duct stent placement in patients undergoing transmural drainage of PFCs is unclear. In a retrospective large-volume series, patients who underwent transpapillary pancreatic duct stent placement and transmural drainage had significantly higher rates of treatment success than those patients who underwent only transmural drainage, 97.5% versus 80%, respectively (28); however, pancreatic duct stent placement may not always be technically feasible as evident from the present study. Gastric outlet obstruction, disconnected duct syndrome, and pancreatic duct strictures/stones can preclude successful stenting (29). In such instances, we undertake only transmural drainage, and if patients have recurrence of PFCs, surgery is recommended as definitive therapy. Although not encountered in the present study, complications of EUS-guided drainage include infection in 2.7%, perforation in 1.3%, and bleeding and stent migration in 0.7% (25). Appropriate use of antibiotics and careful selection of patients (pseudocysts vs walled-off pancreatic necrosis) are important to ensure optimal treatment outcomes.
A recent multicenter study evaluated the role of laparoscopic cystogastrostomy in 10 children with pancreatic pseudocysts (30). The treatment success rate was 92%, time to resumption of oral feeding was 4 days, and the average duration of postprocedure length of hospital stay was 4.5 days. The present study did not evaluate the costs or patient quality of life; however, laparoscopic cystogastrostomy is not widely available, requires considerable expertise, and is operator dependent. In a recent randomized trial in adult patients that compared surgical cystogastrostomy and EUS-guided drainage, although the clinical outcomes were comparable between both the techniques, patients treated with EUS had a significantly better quality of life, shorter length of hospital stay, and the technique was less costly (22). In the present study, the median procedural duration was 12 minutes and the postprocedure length of stay was only 3 days. One of the major advantages of the endoscopic approach over surgery is the timing of the intervention: In several symptomatic children, we intervened as early as 2 weeks and performed transmural stent placement as long as the fluid collection was encapsulated on CT imaging. Given the need to suture, a more mature wall is mandatory and hence the need for a longer waiting time (typically >4–6 weeks) in patients requiring surgical cystogastrostomy.
Despite the advantages outlined above, data on the utilization of EUS for drainage of PFCs in children are scant. The rarity with which these cases are encountered could be a major reason for this impediment. Another logical reason is the lack of skilled endosonographers who are proficient with the technique and “comfortable” to undertake such interventions in children. A technical limitation with EUS is that the therapeutic echoendoscope is 14 mm in diameter and has a rigid tip that restricts its use in extremely young children. Although data are lacking to make any definitive recommendations, we generally reserve the echoendoscope for use in children who are at least older than 18 months. Presently, there are no echoendoscopes designed specifically for use in extremely young children. For ERCPs in this subset of children, we use the specially designed pediatric JPF-7.5 duodenoscope (Olympus America, Center Valley, PA). An algorithmic approach to the management of PFCs in children is shown in Figure 3.
There were several limitations to the present study. One, the series was small and retrospective in nature. Two, all of the procedures were performed by 1 endosonographer (S.V.) at a tertiary referral center, and hence the findings may not be applicable to all centers and endoscopists. Three, we did not evaluate the costs of the procedure or patient quality of life. Nevertheless, despite these limitations, the long-term outcomes appear to be promising. None of the 7 children in this series had PFC recurrence at a median follow-up of nearly 3 years.
In conclusion, preliminary data suggest that EUS-guided drainage is a safe and highly effective technique for the drainage of symptomatic PFCs in children. Larger cohort studies are required to validate these findings. Finally, as EUS gains widespread acceptability, technologic advancements in scope design will be required to meet the needs of all of the sections of this patient population.
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cystogastrostomy; endoscopic drainage; endoscopic ultrasound; endosonography; pancreatic fluid collections; pseudocyst drainage
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