Observational Study
Copyright ©The Author(s) 2018. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Jan 21, 2018; 24(3): 408-414
Published online Jan 21, 2018. doi: 10.3748/wjg.v24.i3.408
Metal stents placement for refractory pancreatic duct stricture in children
In Sook Jeong, Sung Hee Lee, Seak Hee Oh, Do Hyun Park, Kyung Mo Kim
In Sook Jeong, Sung Hee Lee, Seak Hee Oh, Kyung Mo Kim, Department of Pediatrics, University of Ulsan College of Medicine, Asan Medical Center Children’s Hospital, Seoul 05505, South Korea
Do Hyun Park, Department of Internal Medicine, University of Ulsan College of Medicine, Asan Medical Center, Seoul 05505, South Korea
ORCID number: In Sook Jeong (0000-0002-3094-3603); Sung Hee Lee (0000-0003-3262-9658); Seak Hee Oh (0000-0002-9672-8877); Do Hyun Park (0000-0002-0270-6969); Kyung Mo Kim (0000-0001-7896-6751).
Author contributions: Jeong IS, Lee SH, Oh SH and Kim KM contributed to the conception and design of the study; all authors contributed to the study implementation, data acquisition, and data analysis; Jeong IS wrote the manuscript; and all authors contributed to the editing, reviewing, and final approval of the manuscript.
Institutional review board statement: This study was reviewed and approved by the Ethics Committee of Asan Medical Center and University of Ulsan College of Medicine (2017-0210).
Informed consent statement: Patients were not required to provide informed consent for this study because the analysis used anonymous clinical data that were obtained after each patient had agreed to treatment with written consent.
Conflict-of-interest statement: None of the authors have any conflicts of interests to declare.
Data sharing statement: There are no additional data available in relation to this manuscript.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Kyung Mo Kim, MD, Professor, Department of Pediatrics, Asan Medical Center Children’s Hospital, University of Ulsan College of Medicine, 88, Olympic-ro 43-gil, Songpa-gu, Seoul 05505, South Korea. kmkim@amc.seoul.kr
Telephone: +82-2-30103380 Fax: +82-2-4733725
Received: November 10, 2017
Peer-review started: November 11, 2017
First decision: December 13, 2017
Revised: December 20, 2017
Accepted: December 26, 2017
Article in press: December 26, 2017
Published online: January 21, 2018

Abstract
AIM

To evaluate the use of fully covered self-expandable metal stents (FCSEMSs) for pancreatic duct strictures in children with chronic pancreatitis.

METHODS

Eight patients with refractory benign dominant stricture of the main pancreatic duct (MPD) were enrolled through chart reviews between December 2014 and June 2017 in a single center. Endoscopic retrograde cholangiopancreatography (ERCP) with placement of a 6-mm FCSEMS with dual flaps was performed. Endoscopic removal of FCSEMSs was performed with a snare or rat-tooth forceps. All procedures were performed by a pediatric gastroenterologist. For the assessment of outcomes, technical and clinical success, adverse events, and stent patency were evaluated retrospectively.

RESULTS

The placement and removal of the FCSEMSs were successful in all 8 patients. Five patients were boys and 3 were girls. The median age at initial FCSEMS placement was 12 years (range, 5-18 years). The diameters of all the inserted stents were 6 mm, and the lengths were 4-7 cm. The median indwelling time was 6 mo (range, 3-10 mo). No pancreatic sepsis, pancreatitis, cholestasis, or mortality occurred. There was no proximal and distal migration. All subjects showed a patent stent. On follow-up ERCP, the mean diameter of the stricture improved from 1.1 mm to 2.8 mm (P < 0.05), whereas that of upstream dilation improved from 8.4 mm to 6.3 mm (P < 0.05).

CONCLUSION

This initial experience showed that temporary FCSEMS placement is feasible and safe for the management of refractory benign MPD stricture in children.

Key Words: Chronic pancreatitis, Pancreatic duct, Self-expandable metal stent, Child, Endoscopic retrograde cholangiopancreatography

Core tip: This study reports the initial experience with the use of fully covered self-expandable metal stents (FCSEMSs) for recurrent benign pancreatic duct strictures in children. We indwelled 6-mm FCSEMSs with dual flaps in the pancreatic duct of pediatric patients for 6 mo. The placement and removal of the FCSEMSs were technically and clinically successful. There were no adverse events or stent obstruction. The findings support the applicability of FCSEMSs to the pediatric population.



INTRODUCTION

Plastic stents (PSs) or metal stents have been widely used for the management of biliary and pancreatic duct strictures in endoscopic interventions[1]. The fully covered self-expandable metal stent (FCSEMS) was designed to compensate for the defects of PSs and uncovered self-expandable metal stents (SEMSs). The SEMS has the advantages of longer patency and resolution of main pancreatic duct (MPD) strictures because its lumen diameter is larger than that of the PS[2,3]. Meanwhile, the FCSEMS has been shown to improve tissue embedding by wrapping around the frame of the uncovered SEMSs[4].

As SEMSs were initially used for malignant biliary obstruction[5], FCSEMSs have been widely used for the management of biliary and pancreatic duct strictures in adults[6]. FCSEMSs have proven to be a particularly useful intervention for malignant biliary obstruction[7,8], and their use in the management of benign biliary strictures has been expanding steadily[9]. In recent studies, FCSEMSs were increasingly used for the management of MPD strictures refractory to PS placement in adults[10].

In general, studies on the application of stents in pediatric patients are lacking. However, most pediatric studies of endoscopic retrograde cholangiopancreatography (ERCP), including our previous study, investigated the use of PSs; therefore, stenting is an important indication in pediatric ERCP[11-13]. One pediatric study showed that PS placement was effective for reducing the recurrence of pancreatitis[14].

For these reasons, FCSEMSs may be useful even in pediatric populations. In this study, we evaluated the feasibility, safety, and therapeutic effect of FCSEMSs for the management of benign MPD strictures in pediatric patients with chronic pancreatitis (CP).

MATERIALS AND METHODS
Patients

This was a retrospective study of data collected through medical chart reviews between December 2014 and June 2017 at Asan Medical Center Children’s Hospital in Seoul, South Korea. Eight patients with CP and benign dominant MPD stricture refractory to PS placement were enrolled (Table 1). Patients with MPD dilatation due to a malignant cause or trauma were excluded. Five patients were boys and 3 were girls. Their median age was 12 years (range, 5-18 years). The patients in this study had pancreatic divisum and/or gene mutations. The genetic mutations were PRSS1 p.Gly208Ala, PRSS1 p.Arg122His, SPINK1 p.Asn34Ser, SPINK1 p.ThrT53Ilefs*41, SPINK1 IVS3(+2)T>C, and CFTR p.Gln1352His. The strictures were located at the pancreatic head in 5 patients, at the pancreatic neck in 2 patients, and at the pancreatic body in 1 patient. The subjects had a history of previous PS trials after endoscopic sphincterotomy. The median number of days and total duration of PS placement were 2 d (range, 1-7 d) and 57 d (range, 1-431 d), respectively. The stricture was verified using imaging methods [ultrasonography, computed tomography, endoscopic retrograde pancreatography (ERP), or magnetic resonance cholangiography]. A dominant stricture was defined when the contrast medium on the ERP film was not washed out and the upstream MPD dilation was ≥ 6 mm in diameter[15].

Table 1 Baseline characteristics of the 8 patients with refractory benign dominant main pancreatic duct strictures treated with a fully covered self-expandable metal stent.
Case no.SexAnatomical abnormalityGenetic mutationNo. of previous plastic1 stent placementsPlacement time for each plastic stent (d), median (range)Age at first insertion of a FCSEMS (yr)Location of the strictureDiameter and length of the stent (mm/cm)
1FPancreas divisumPRSS1225.5 (19-32)17Head6/4
2M-SPINK1742.0 (4-93)12Head6/5
3MIncomplete pancreas divisum-4126.5 (63-431)10Head6/6
4MPancreas divisumCFTR357.0 (1-109)12Body6/7
5F-PRSS1146.018Neck6/7
6M-PRSS1258 (24-92)5Head6/4
7F-SPINK11879Head6/4
8M-SPINK112916Neck6/7
Procedure

The first session of placement and removal of FCSEMS was performed by an adult and pediatric gastroenterologist. Thereafter, all procedures were performed by a pediatric gastroenterologist. ERP was performed using either an adult duodenoscope (JF; Olympus Optical, Tokyo, Japan) or a therapeutic duodenoscope (TJF, Olympus Optical, Tokyo, Japan). Commercially available 6-mm FCSEMSs (Hanarostent Biliary dual flap; M.I. Tech, Seoul, South Korea) that consisted of nitinol material with a silicone covering membrane were used (Figure 1). After the endoscopic sphincterotomy, which had been described elsewhere, dilatation of the stricture was performed with a Soehendra stent retriever (Wilson Cook Medical, Winston-Salem, NC, United States) and/or a Hurricane dilator balloon (Boston Scientific, Natick, MA, United States) prior to stent placement. The insertion length of the stent was determined such that at least 1 cm of ampulla and normal area at the end of the stenosis were each covered. Repositioning was carried out until the stent was fully inflated and placed in the targeted location. On the basis of previous studies in adults[16], stent removal was planned with rat-tooth forceps at 6 mo after placement, unless adverse events or episodes of pancreatitis had occurred. Informed consent was obtained from the parents of the patients, after the risks and benefits of the procedure and alternative treatments were explained. The study protocol was approved by the institutional review board of Asan Medical Center (2017-0210).

Figure 1
Figure 1 The fully covered self-expandable metal stent with 3 flaps at both ends used in this study (Hanarostent Biliary dual flap; M. I. Tech, Seoul, South Korea). A and B: The border between the gray and yellow points, shown by the blue arrows, marks the end of the stent. C: Small red arrow heads indicate the flaps.
Measurement of outcome

Feasibility was evaluated in terms of technical success, migration, and patency. Technical success was determined in accordance with the success of stent placement and removal. Successful stenting was attained when the stent passed through the stricture and the mesh spread easily, followed by a flow of pancreatic juice or washing fluid into the lumen of the stent. Successful removal was attained when the entire stent was removed without ductal leakage during contrast medium injection. Stent patency was assessed via visual inspection when the FCSEMS was removed. Efficacy was evaluated according to the improvements of the stricture and reduction of pancreatic pain and pancreatitis. Stricture improvement was evaluated by measuring the diameter of the stricture and the upstream dilation of the MPD as shown on pancreatography after the removal of the first metal stent. Safety was evaluated based on the occurrence of adverse events such as pancreatitis, cholestasis, bowel perforation, sepsis, or mortality. Blood pressure, heart rate, body temperature, laboratory tests (complete blood count and C-reactive protein, total bilirubin, direct bilirubin, amylase, and lipase levels), and abdominal radiographs were conducted at 3 d and 14-21 d after FCSEMS placement to evaluate for short-term adverse events.

Statistical analyses

The Wilcoxon signed-rank test was used to compare changes in the diameter of the pancreatic duct between pre- and post-FCSEMS measurements. The IBM SPSS Statistics ver. 23.0 (IBM Co., Armonk, NY, United States) software was used for statistical analysis, and the stenting duration and patency are expressed as median values and ranges. P values < 0.05 were considered statistically significant.

RESULTS
Evaluation of feasibility

In all 8 patients, the placement of the FCSEMS with dual flaps was technically successful. The diameters of all inserted stents were 6 mm, and the lengths were 4-7 cm. The stents were successfully removed in all patients. The median indwelling time of stenting was 6 mo (range, 3-10 mo; Table 2). One patient had the stent removed 4 mo later than the planned time of removal because of personal reasons. However, stent embedding and occlusion did not develop (Figure 2). The patency of the stent lumen in the 8 patients with an FCSEMS had been maintained upon assessment at the time of stent removal. No stent migrations were observed.

Table 2 Resolution of pancreatic duct strictures after the first placement of a fully covered self-expandable metal stent.
Case no.Duration of stenting (mo)Diameter of the stricture (cm)
Diameter of the dilated segment1 (cm)
PrePostPrePost
130.83.06.54.9
2101.52.012.18.7
361.23.411.37.1
460.93.48.16.4
561.04.47.15.0
660.90.96.05.2
761.62.19.46.1
860.83.07.07.0
mean ± SD621.1 ± 0.32.8 ± 0.98.4 ± 2.56.3 ± 1.6
P valueNA0.0170.018
Figure 2
Figure 2 Endoscopic retrograde pancreatography images for case 3. A: Pancreatography image showing a pancreatic duct stricture in the pancreatic neck before the insertion of the fully covered self-expandable metal stent (FCSEMS). B and C: An FCSEMS with flaps placed through the narrow pancreatic duct. D: The stent lumen showing patency at 6 mo after FCSEMS placement.
Evaluation of efficacy

Recurrent pancreatitis and pancreatic pain did not develop in 4 patients during FCSEMS placement. In 1 patient, pain developed 3 mo after stenting, resulting in an early removal that revealed remnant stones blocking the distal MPD, although the lumen of the FCSEMS was patent. Following the removal of the stone and reinsertion of the stent, the pain disappeared and statistically significant improvements in stricture and upstream dilation were observed. The mean stricture diameter was 1.1 ± 0.3 cm before stenting and 2.8 ± 0.9 cm after stenting (P < 0.05). The diameter of the upstream dilatation showed improvement from 8.4 ± 2.5 cm to 6.3 ± 1.6 cm after stenting (P < 0.05).

Safety

No adverse events such as pancreatitis, cholestasis, sepsis, bowel perforation, or mortality occurred during FCSEMS placement (Table 3).

Table 3 Feasibility and safety of the placement of a fully covered self-expandable metal stent based on the occurrence of adverse events.
Case no.Stent migrationStent patencyPancreatitisCholestasisBowel perforationSepsisMortality
1NYNNNNN
2NYNNNNN
3NYNNNNN
4NYNNNNN
5NYNNNNN
6NYNNNNN
7NYNNNNN
8NYNNNNN
DISCUSSION

We, herein, report the first case series of the use of FCSEMSs in pediatric patients with CP and MPD strictures refractory to PS placement. Despite the small sample size and lack of long-term follow-up, this preliminary study presents evidence of the feasibility of the use of FCSEMS even in children, with technical and functional success. The disadvantages of PSs include migration and occlusion by sludge, resulting in necessary replacement at around 3 mo[17]. In a previous study, FCSEMSs in the management of MPD stricture showed efficacy and safety at 6-mo intervals in adults[16]. We suggest that our short-term outcomes are similar to the results for adults in terms of the improvement of strictures and the safety of the procedure[17]. Uncovered SEMSs are associated with tissue ingrowth through the stent mesh, which makes their removal difficult[18]. Tissue hyperplasia was reported in 23% of patients with partially covered stents[19]. When the stent was pulled using rat-tooth forceps at the scheduled removal time, the stent moved easily out of the pancreatic duct without resistance.

Initially, the introduction of FCSEMSs solved the tissue ingrowth issue but led to greater stent migration, with an incidence as high as 41%[20]. To overcome this challenge, fins and flaps have been incorporated into these devices[8,21]. During our procedure with a dual-flapped FCSEMS, we did not encounter any bleeding, ulcers, or migration problems. In terms of bioavailability, the nitinol materials and silicone membranes of the FCSEMSs applied in the present study series have been used safely in a previous study on the drainage of walled-off necrosis in children[22].

The major cause of CP in pediatric patients is hereditary pancreatitis rather than gallstones and alcoholism[23,24]. Furthermore, because the pancreas reserve of pediatric patients may worsen over time, considering total pancreatectomy with autologous islet transplantation (TP-IAT) may be much more important in children[25]. Surgery can result in a reduction of chronic pain through TP-IAT, which was shown to have a more protective effect against negative developments such as postoperative diabetes in preadolescence[26]. However, insulin dependency was still present in approximately 40% of postoperative patients[27]. Surgical burdens including morbidity, gastric motility dysfunction, and endocrine and exocrine replacement may also occur[28,29]. Given that the cause of CP differs between adults and children, adult guidelines for treating this condition as well as surgical recommendations cannot be automatically applied to pediatric cases. Therefore, until these problems are definitively resolved, endoscopic rather than surgical treatment should be considered in children.

In conclusion, this study showed that the use of FCSEMSs is feasible and safe and may be effective for the management of children with refractory benign MPD strictures. A future long-term investigation with a greater number of patients is warranted.

ARTICLE HIGHLIGHTS
Research background

Plastic stents (PSs) or metal stents have been widely used for the management of biliary and pancreatic duct strictures in endoscopic interventions. The fully covered self-expandable metal stent (FCSEMS) was designed to compensate for the defects of PSs and uncovered self-expandable metal stents (SEMSs). FCSEMSs have been widely used for the management of biliary and pancreatic duct strictures in adults. In general, studies on the application of stents in pediatric patients are lacking. This study reported our experience with using FCSEMS as part of the treatment for benign main pancreatic duct (MPD) strictures in pediatric patients with chronic pancreatitis (CP).

Research motivation

The major cause of CP in pediatric patients is hereditary pancreatitis rather than gallstones and alcoholism, unlike in adults. Pediatric patients experience mental and physical repetitive pain from complications of MPD stricture during their long life. Stenting is an important indication in pediatric ERCP. In a previous study, the use of FCSEMSs in the management of MPD stricture showed efficacy and safety at 6-mo intervals in adults. We report that our short-term outcomes in children are similar to the results obtained for adults, in terms of the improvement of strictures and the safety of the procedure.

Research objectives

This study evaluated the feasibility, safety, and therapeutic effect of FCSEMSs for the management of benign MPD strictures in pediatric patients with CP.

Research methods

This was a retrospective study of data collected through medical chart reviews between December 2014 and June 2017 at Asan Medical Center Children’s Hospital in Seoul, Korea. Eight patients with CP and benign dominant MPD stricture refractory to PS placement were enrolled. A dominant stricture was defined when the contrast medium on the endoscopic retrograde pancreatography film was not washed out and the upstream MPD dilation was ≥ 6 mm in diameter. Feasibility was evaluated based on technical success, migration, and patency. Technical success was determined in accordance with the success of stent placement and removal. Stricture improvement was evaluated by measuring the diameter of the stricture and the upstream dilation of the MPD. Safety was evaluated based on the occurrence of adverse events at 3 d and 14-21 d after FCSEMS placement. The Wilcoxon signed-rank test was used to compare changes in the diameter of the pancreatic duct between pre- and post-FCSEMS measurements. The IBM SPSS Statistics ver. 23.0 software was used for statistical analysis, and the stenting duration and patency are expressed as median values and ranges.

Research results

In all 8 patients, the placement of the 6-mm FCSEMS with dual flaps was technically successful. The median indwelling time of stenting was 6 mo (range, 3-10 mo). Stent embedding and occlusion did not develop. The patency of the stent lumen in the 8 patients with an FCSEMS had been maintained upon assessment at the time of stent removal. No stent migrations, adverse events, and mortalities were observed. After the removal of the stone and insertion of the stent, the pain disappeared and statistically significant improvements in stricture and upstream dilation were observed. The mean stricture diameter was 1.1 ± 0.3 cm before stenting and 2.8 ± 0.9 cm after stenting (P < 0.05). The diameter of the upstream dilatation showed improvement from 8.4 ± 2.5 cm to 6.3 ± 1.6 cm after stenting (P < 0.05). A future study with a larger sample size could clarify the usefulness of FCSEMS in children with benign MPD dilatation.

Research conclusions

This is the first study to investigate the efficacy and safety of the placement of the 6-mm FCSEMS with dual flaps in children. Despite the technical success and satisfactory clinical outcomes in these 8 children, the present study had certain limitations, including its retrospective design, relatively small sample size, and short follow-up period. In this study, we report our experience with using FCSEMS as part of the management of benign MPD strictures in pediatric patients with CP, providing valuable information about useful treatment for such patients. FCSEMS placement is an effective and safe management strategy for MPD strictures in pediatric patients with CP.

Research perspectives

We report the first case series of the use of FCSEMSs in the pediatric population with CP and MPD strictures refractory to PS placement. Despite the small sample size and lack of long-term follow-up, this preliminary study presents evidence of the feasibility of using FCSEMS even in children, with technical and functional success. A future long-term investigation with a greater number of patients is warranted.

Footnotes

Manuscript source: Unsolicited manuscript

Specialty type: Gastroenterology and hepatology

Country of origin: South Korea

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P- Reviewer: Fu D S- Editor: Gong ZM L- Editor: A E- Editor: Huang Y

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