Gastrointestinal Intervention 2018; 7(2): 52-56  https://doi.org/10.18528/gii180013
Usefulness of stent placement above the papilla, so-called, ‘inside stent’
Tanyaporn Chantarojanasiri1,* , Hirofumi Kogure2, Tsuyoshi Hamada2, Yousuke Nakai2, and Hiroyuki Isayama3
1Department of Internal Medicine, Police General Hospital, Bangkok, Thailand, 2Department of Gastroenterology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan, 3Department of Gastroenterology, Graduate School of Medicine, Juntendo University, Tokyo, Japan
*Department of Internal Medicine, Police General Hospital, 492/1 Rama 1 Road, Pathumwan, Bangkok 10330, Thailand. E-mail address:chtunya@gmail.com (T. Chantarojanasiri). ORCID: https://orcid.org/0000-0001-5781-8696
Received: April 23, 2018; Accepted: June 19, 2018; Published online: July 31, 2018.
© Society of Gastrointestinal Intervention. All rights reserved.

cc This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Stent occlusion and cholangitis are common complications after endoscopic biliary stenting caused by duodenobiliary refluxes and food impaction. To prolong the stent patency, the concept of stenting above the papilla, so-called inside stent, has been developed. Various studies of the inside stent in the treatment of both benign and malignant biliary obstruction have been published, with a promising result. However, most studies were retrospective, with wide variation of stent type and the etiology of biliary obstruction. This review aims to summarize the principle, evidence, and the usefulness of inside biliary stent.

Keywords: Cholestasis, Extrahepatic, Stent
Introduction

Endoscopic biliary stenting has been one of the main treatments of the biliary obstruction, both in malignant and benign conditions. However, stent occlusion leading to biliary obstruction, and ascending cholangitis are the major complications that necessitate stent replacement and repeated endoscopic interventions. These complications might impact the patients’ survival, especially in those receiving immunosuppressive therapy for malignant biliary obstruction or after liver transplantation. As a result, various methods and stent design to prolong the stent patency and reduce such complications were developed, with placing a stent above the papilla as one of the methods being used, especially in patients after liver transplantation.1

This review aims to summarize the concepts and clinical application of biliary stenting above the papilla as well as related evidences. Literature search though PubMed using keywords; inside stent, biliary, stent above papilla, as well as related literatures were reviewed. In this review article, we discussed about both plastic and metallic stent.

From Fact to Theory

Transpapillary plastic biliary stent could be occluded by several causes, such as bile sludge, bacteria, fibrin, dietary fiber and inflammatory cells, which could be partially occluded as early as first week after stent placement.2,3 On the other hand, after transpapillary self-expandable metallic stent placement, duodenobiliary refluxes usually occurs.4 These findings lead to the concept of placing the stent above papilla.

Placing the stent above papilla might promote the longer patency of the stent by several mechanisms. Firstly, keeping the papilla as the natural orifice might prevent the duodenobiliary refluxes. This would reduce the sludge formation inside the stent which results from enteric bacterial colonization. Secondly, using a shorter stent might reduce the chance of cholangitis in undrain segment due to the obstructed side branches. Finally, placing a stent above the papilla might prevent stent occlusion from food impaction at the duodenal end (Fig. 1).

Duodenobiliary Reflux

Ascending infection from duodenal content reflux is one of the important mechanism of the ascending cholangitis. As mentioned earlier, reflux of duodenal content was demonstrated in most patients after receiving transpapillary metallic stent but cholangitis occurred only in the presence of stent obstruction.4 Animal studies showed that the incidence of ascending cholangitis and bacterial contamination of the bile duct increased after transpapillary stenting and papillotomy.5,6 Moreover, increasing bacterial biofilm in those without sphincteric barrier leads to more rapid development of biliary stones and sludges formation.7 Another in vitro study also showed that stent blockade was associated with internal colonization of anaerobic bacteria, especially in those received prophylactic antibiotics.8

The proof-of-concept studies for duodenobiliary refluxes in the natural history of patients with malignant biliary obstruction underwent biliary stenting have been demonstrated, using specially design metallic stent with antireflux property.9,10 Recent randomized controlled trial (RCT) using metal stents with antireflux property in patients with malignant distal common bile duct (CBD) obstruction also shown longer stent patency and decrease risk of ascending cholangitis. However, this did not improved the patients’ survival.11 Another study also showed superior stent patency time but no difference in sludge formation when compared between metallic stent with anti-reflux property with the conventional fully cover metallic stent.12 These results may imply that there might be other factors rather than the reflux that promote sludge formation.

On the other hand, apart from studies using specially design antireflux stent, several studies of stenting above the papilla, so-called ‘inside stent’, that keep the papilla as the natural barrier as anti-reflux valves have been published.

Clinical Applications of Stenting above the Papilla

The benefit of stenting above the papilla was demonstrated in patients with malignant and benign biliary stricture after orthotropic liver transplantation.1 In most report, the stent insertion was performed without sphincterotomy to preserve the papillary function.13,14 However, some author suggested sphincterotomy should be performed if a larger stent would be inserted as post-procedure pancreatitis was observed after placement of 10 Fr plastic stent.15 As the distal end of the stents did not cross the ampulla and compress the pancreatic duct opening, as many stent could be inserted as needed without performing the sphincterotomy. Later, this so-called ‘inside stent’ also demonstrated its’ usefulness in both hilar and lower bile duct obstruction. The stent could be inserted either endoscopically or by transcutaneous intervention.16 In those with distal bile duct obstruction, the distance of 15 mm between the papilla and the stricture was required for the inside stent placement both for plastic and metallic stenting.15,17,18 In one retrospective study, clearance length of 1 to 2 cm is required for the placement of inside stent and 30° to 50° flexion for plastic stent is recommended to prevent stent migration.19

Benign Biliary Stricture

In early reports, plastic stenting above the papilla has been used in patients with post-liver transplant biliary stricture to reduce the duodenobiliary reflux, reduce food clogging of the stent, and prevent excessive normal CBD stenting.13,18,2023 In most reports, usual straight biliary stents were modified by attaching a knotted nylon thread to ease the stent removal and, in some study the distal flap was removed to ease the stent insertion (Fig. 2).13,22,23 In some study, plastic stent insertion also demonstrated a good result in cases with post-transplant biliary leakage.23 Summary of studies (not including case reports) of inside stenting for benign biliary stricture is demonstrated in Table 1.13,18,22,23

Malignant Biliary Stricture

The first RCT using plastic stent in malignant biliary obstruction did not shown clinically significant benefit of prolonged stent patency in those receiving inside stent.24 Not only for biliary drainage, the inside stent also demonstrated a good result as a salvage therapy for obstructed metallic stent caused by tumor overgrowth25 and as the bridging treatment before neoadjuvant chemotherapy.26

In a retrospective study, longer stent patency was seen in those received stent insertion above the papilla as a palliation for malignant distal CBD stricture.7 Despite the concern for stent migration using a shorter metallic stent, there has been several studies reporting efficacy and low complication of the intraductal stenting using short-fully covered metallic stent, both in post-transplant and in malignant biliary obstruction (Fig. 3).18,20,27 Another retrospective study in patients with malignant biliary obstruction also shown increased rate of cholangitis in those received metallic stent placement across the duodenal papilla. This report also emphasized efforts to preserved the papillary function.28 Summary of studies (not including case reports) of inside stenting for malignant biliary stricture is demonstrated in Table 2.1517,2428

Who Should Benefit from Placing the Inside Stent?

According to the proposed mechanism of placing inside stent, this technique should be most useful in those with high chance of duodenobiliary reflux such as cases with duodenal obstruction distal to the bile duct opening or dysmotility. In such cases, the retained content in the proximal duodenum might reflux into the bile duct through the stent, causing frequent cholangitis and rapid stent obstruction. A multicenter study also demonstrated the risk of biliary stent dysfunction become higher in those received duodenal stent placement due to food impaction and non-occlusion cholangitis.29

Also, another study showed that placing a transpapillary stent in patients with indwelling duodenal stent results in a shorter stent patency compared to those receiving transmural approach.30 This might be due to increase duodenobiliary refluxes by the placement of duodenal stent. In such cases placing inside stent might be more beneficial. As mentioned earlier, the placement of inside stent could be performed in cases that the lesion is located 1 or 2 cm above the papilla.

Metallic or Plastic?

There has been no comparison study whether to use the plastic or metallic stent. Similar to usual biliary stenting, repeated endoscopic retrograde cholangiopancreatography procedure is necessary in those receiving plastic stent and fully covered self-expandable metal stent (FCSEMS) inside stent placement. However, in those with hilar obstruction, FCSEMS is not recommended as the membrane might obstruct other biliary branches. Studies using bare SEMS in hilar and non-hilar obstruction were reported16,28 but the number of cases and long term outcome data are still limited.

EST or No EST

Despite the concept of preserving the papillary function, there have been a few studies that endoscopic sphincterotomy (EST) was performed prior to the stent insertion. These studies included both using the plastic and the metallic stent. In a report using plastic stent, EST was performed only in cases that 10 Fr stent would be inserted as the authors experienced a case of acute pancreatitis following 10 Fr plastic stent insertion.15 On the contrary, other reports using plastic stent with larger diameter (12 Fr) did not report the same finding. However, the number of cases using 12 Fr stents might be too small to demonstrate any significant difference as most reports were retrospective case series. In the studies using metallic stent, EST was performed in those using dedicated FCSEMS with lasso.18,27 In these studies, EST might be necessary to facilitate the FCSEMS removal. Based on abovementioned evidences, whether to perform EST is still controversial but may be performed depends on the stent type.

Troubleshooting in Placing Inside Stent

One of the problems after placing inside stent is stent or string upward migration. In our experience, inside stent with inwardly migrated suture could be easily removed using the rotatable basket grasping the suture inside the bile duct. However, by only grasping the suture, the power to retrieve the stent is low. Other options included grasping the suture near the stent body or grasping the stent directly using rotatable basket and remove in the same fashion as removing a migrated stent.

In cases that the biliary stricture is very tight, passing the guidewire through the stricture might be difficult. In such case, the stent exchange could be performed by passing the guidewire through the previous stent lumen and remove the in situ stent using stent retriever, so-called, ‘wire-guided exchange technique’.31

Summary

Inside stent has promising role in the treatment of both benign and malignant biliary stricture. By preserving the papilla function as the barrier for duodenobiliary refluxes, longer stent patency was observed in many studies. Recent development of dedicated metallic stents for placing above the papilla also yields a promising result.

Conflicts of Interest

No potential conflict of interest relevant to this article was reported.

Figures
Fig. 1. The concept of placing a stent above the papilla. With the natural papilla functioning as a barrier for duodenal refluxes and food impaction, placing a stent above the papilla (A) should prolonged the stent patency compared with conventionally placing a stent with the distal end inside the duodenum (B).
Fig. 2. Biliary anastomotic stricture after left-liver living donor liver transplantation. (A) The ThroughPass-iS (Gadelius Medical, Tokyo, Japan) in which the suture thread is tied to the distal end of the stent. (B) Endoscopic retrograde cholangiography showing an inside stent placed across the stricture. (C) Endoscopic image of the papilla after inside stent deployment; the nylon thread is visible.
Fig. 3. Biliary anastomotic strictures after right-liver living donor liver transplantation. In this case, a fully covered self-expandable metallic stent (Kaffes Biliary Stent; Taewoong Medical, Seoul, Korea) (A) was inserted. The stent has a waist at the middle portion as an anti-migration system and a long, platinum, radiopaque-marked retrieval string. (B) Endoscopic retrograde cholangiography showing two Kaffes stents placed across the strictures. (C) Endoscopic view of the papilla; the platinum, radiopaque-marked retrieval strings are visible.
Tables

Table 1

Summary of the Study Using Inside Stent for Benign Biliary Obstruction

Author (year)Study designNo. of patients (total/inside stent)Type of stent (size)Cause and site of biliary obstructionPapilla statusResult
Hisatsune et al13 (2003)Retrospective26/14Amsterdam type with thread (7–12 Fr)Benign, posttransplantIntactAverage patency 450 days 36% delayed complication (migration and occlusion)
Yazumi et al23 (2006)Retrospective75/55Tannenbaum, Amsterdam type with thread (7–12 Fr)Benign, posttransplantIntact68% success for anastomotic stricture and 50% success for bile leak
Moon et al18 (2012)Prospective feasibility study21/21FCSEMS with lasso (8–10 mm × 3–7 cm)Benign, any siteESTFeasibility with 95.2% clinical success
Kurita et al22 (2013)Retrospective118/92Plastic stent with thread (10–12 Fr)Benign, posttransplantIntact88% success 22.3% complication (pancreatitis, cholangitis)

FCSEMS, fully covered self-expandable metal stent; EST, endoscopic sphincterotomy.

Table 2

Summary of the Study Using Inside Stent for Malignant Biliary Obstruction

Author (year)Study designNo. of patients (total/inside stent)Type of stent (size)Cause and site of biliary obstructionPapilla statusResult
Pedersen et al24 (1998)RCT34/17Teflon straight (10 Fr)Malignant CBD obstructionN/ANo significant difference in stent patency
Uchida et al17 (2005)RCT32/16Tannenbaum (10 Fr)Malignant, non-hilarN/ALonger stent patency in inside stent
Okamoto et al28 (2006)Retrospective108/71Bare and FCSEMSMalignant, any siteN/ALess cholangitis in inside stent
Inatomi et al25 (2013)Retrospective42/12Conventional plastic stent with thread (7 Fr)Malignant, hilarIntactSimilar patency compared with MS, better as a salvage therapy for occluded MS
Huang et al16 (2015)*Retrospective98/47Bare SEMS (8–10 mm × 4–10 cm)Malignant, non-hilarIntactLonger patency and less infection than those placed across papilla
Kobayashi et al15 (2015)Retrospective57/25Tannenbaum, Amsterdam type with thread (7–10 Fr)MalignantEST only before placing 10 Fr stentLess stent obstruction in inside stent
Kubota et al26 (2016)Retrospective40/17Plastic stent with thread (7 Fr)Malignant, hilarIntactInside stent provide longer patency in patient received neoadjuvant chemotherapy
Choi et al27 (2016)Prospective feasibility study51/51FCSEMS with lasso (8–12 mm × 3–7 cm)Malignant, non-hilarSmall EST98% clinical success, mean stent patiency 297 days

RCT, randomized controlled trial; CBD, common bile duct; N/A, not mentioned; FCSEMS, fully covered self-expandable metal stent; MS, metallic stent; SEMS, self-expandable metal stent; EST, endoscopic sphincterotomy.

*Percutaneous approach.

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