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Keywords:

  • biliary stenting;
  • endoscopic retrograde cholangiopancreatography (ERCP);
  • malignant biliary obstruction;
  • self-expandable metallic stent (SEMS)

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Strategy of Biliary Stenting
  5. Distal Bile Duct Strictures
  6. Hilar Bile Duct Strictures
  7. Conclusions
  8. Acknowledgments
  9. Conflict of Interests
  10. References

In the present review, we describe the current status of biliary stenting in patients with unresectable malignant biliary strictures. Self-expandable metallic stents (SEMS) are the ideal biliary stent for both distal and hilar biliary strictures, although in terms of distal biliary strictures, there is still some debate as to the selection of covered or uncovered SEMS, suprapapillary or transpapillary stent placement, side-by-side or stent-in-stent placement, unilateral or bilateral stent placement and thenecessity for sphincterotomy. Further high-quality randomized controlled trials for these procedures are warranted.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Strategy of Biliary Stenting
  5. Distal Bile Duct Strictures
  6. Hilar Bile Duct Strictures
  7. Conclusions
  8. Acknowledgments
  9. Conflict of Interests
  10. References

Since Sohendra and Reynders-Frederix[1] introduced transpapillary biliary drainage in 1980, stenting has become widespread and is now the standard treatment for malignant biliary strictures. As 32 years has passed, there have been various changes from the initial plastic stents (PS) to large-bore plastic stents, non-expandable metallic stents, and self-expandable metallic stents (SEMS). Two decades ago, SEMS meant uncovered SEMS, but, currently, there are various types of SEMS, such as SEMS with partially or fully covering materials, internal stents, anti-migration types such as flare-, profession-surfaced, anchoring type, and anti-reflux valve stents. Furthermore, recently, bioabsorbable or biodegradable stents[2] have been developed. Here, we review biliary stenting for the treatment of unresectable malignant biliary obstruction.

Strategy of Biliary Stenting

  1. Top of page
  2. Abstract
  3. Introduction
  4. Strategy of Biliary Stenting
  5. Distal Bile Duct Strictures
  6. Hilar Bile Duct Strictures
  7. Conclusions
  8. Acknowledgments
  9. Conflict of Interests
  10. References

Various types of plastic stents and SEMS are now commercially available. In addition to stent characteristics, there are several factors affecting the choice of biliary stent; for example, prognosis of patient, cause/site/length of stricture, diameter of the bile duct, site of the cystic duct, presence of an intact pancreatic duct, and multi-disciplinary therapies such as chemoradiation therapy. Based on several factors, stents are usually selected for the best therapy of each patient. Therefore, biliary endoscopists should know the characteristics of the various types of stent and the evidence available for the best use of each type.

Distal Bile Duct Strictures

  1. Top of page
  2. Abstract
  3. Introduction
  4. Strategy of Biliary Stenting
  5. Distal Bile Duct Strictures
  6. Hilar Bile Duct Strictures
  7. Conclusions
  8. Acknowledgments
  9. Conflict of Interests
  10. References

Plastic stent versus SEMS

Theoretically, large-bore SEMS show long patency compared with plastic stents (Fig. 1). To date, several randomized control trials have been done comparing PS with SEMS for palliation of malignant distal biliary obstruction and these are shown in Table 1.[3-9] Although the technical placement success rates for both stents were similar, the occlusion rate of plastic stents is higher than that of SEMS. As a result, plastic stent patency is statistically shorter than that of SEMS.

figure

Figure 1. Plastic stents. Straight and double pigtail types.

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Table 1. RCT comparing PS with SEMS for palliation of malignant distal biliary obstruction
AuthorNo. patientsSuccess drainage (%)Occlusion rate (%)Stent patencyP-value
PSSEMSPSSEMSPSSEMSPSSEMS
  1. d, day; mo, month; NA, not available; PS, plastic stent; RCT, randomized controlled trials; SEMS, self-expandable metallic stent.

Davids et al.[3]495695965433126 d273 d0.006
Carr-Locke et al.[4]78869598131362 d111 dNA
Knyrim et al.[5]31311001003622140 d189 d0.035
Kaassis et al.[6]5959NANA6320165 dNA0.007
Soderlund and Linder[7]51491009643181.8 mo3.6 mo0.0006
Isayama et al.[8]53521001005935130 d419 d0.026
Choi et al.[9]2321100100NANA94.6 d223.6 d0.006

Partially/fully covered versus uncovered SEMS

Partially, fully covered and uncovered SEMS are shown in Figure 2 and the characteristics of the three types of SEMS are shown in Table 2. As uncovered SEMS have a lower shortening rate (<5%), stent deployment is relatively easier than for covered SEMS (approximately 20–40% shortening). In addition, they can be used for hilar biliary strictures. However, uncovered SEMS permit tumor ingrowth through the mesh, resulting in early stent occlusion. In contrast, although the covering around the metal stent prevents tumor ingrowth, leading to longer stent patency, compression of the pancreatic duct orifice at the papilla and cystic duct can occasionally cause stent-induced acute pancreatitis or acute cholecystitis. Furthermore, covered SEMS are likely to have more inward or outward migration than uncovered SEMS. This means the possible need for stent removal using biopsy forceps or snare forceps. From the aspect of stent removal, fully covered SEMS can be easily removed compared with partially covered SEMS because of less overgrowth. A comparison of the outcomes between transpapillary covered and uncovered SEMS stenting is shown in Table 3.[10-18] Most reports, including retrospective studies and randomized controlled trials (RCT), showed no statistically significant difference in stent patency or time to stent dysfunction. Of three RCT, two[17, 18] revealed no statistically significant difference in patency between covered and uncovered SEMS but one[14] showed better patency in the covered stents. In addition, covered SEMS showed a higher complication rate than uncovered SEMS.

figure

Figure 2. Metal stents. (a) Uncovered metal stent (X-Suit NIR; Olympus Medical Systems, Tokyo, Japan). (b) Partially covered metal stent (Niti-S Comvi stent; Taewoong Medical, Seoul, Korea). (c) Fully covered metal stent (WallFlex; Boston Scientific Japan, Tokyo, Japan).

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Table 2. Characteristics of current covered and uncovered metal stents
Type of stentAdvantagesDisadvantages
Uncovered metal stent

Easy deployment (lower shortening rate)

Available hilar portion thinner

Introducer

Stent obstruction

 tumor ingrowth

 tumor overgrowth

Partially covered metal stent

Prevention of tumor ingrowth

Possible removal

Stent obstruction

 tumor overgrowth

Complications

 migration/dislocation

 pancreatitis

 cholecystitis

Fully covered metal stent

Prevention of tumor ingrowth

High possibility of removal

Complications

 migration/dislocation

 pancreatitis

 cholecystitis

Table 3. Comparison of transpapillary covered and uncovered metal stents
AuthorStudy designNo. patients (n)Stent patency or Time to obstruction/dysfunction (days)Stent occlusion (n)Tumor ingrowth (n)Migration (n)Cholecystitis (n)Pancreatitis (n)
UCUCUCUCUCUCUC
  1. *P < 0.05.

  2. C, covered metal stent; NA, not available; R, retrospective study; RCT, randomized controlled trial; U, uncovered metal stent.

Smits et al.[10]R2422NANA322001    
Shim et al.[11]R26212332676262      
Nakamura et al.[12]R1013>402>4702120 11010
Miyayama et al.[13]R1922NANA143NANA 10215
Isayama et al.[14]RCT5557166*304*218160010215
Park do et al.[15]R981081491442120170062%2%26
Yoon et al.[16]R364120224515950120100
Telford et al.[17]RCT6168711357112086087%7%10
Kullman et al.[18]RCT191188199154353921*9062243

A recent meta-analysis of five randomized trials involving 781 patients comparing covered and uncovered SEMS revealed that covered SEMS provided a significantly longer duration of patency than uncovered stents. These data may promote the use of covered SEMS over uncovered stents for palliation of malignant distal biliary obstruction and may potentially decrease the need for reintervention.[19] However, there are several issues in that study: (i) the low number of studies available; (ii) two of the five studies were from one institution;[19] and (iii) the study included two percutaneous transhepatic biliary stenting studies among all five randomized trials. Interestingly, the latest meta-analysis revealed that the use of covered SEMS, compared with uncovered SEMS, in patients with distal malignant biliary obstruction is of unclear benefit; covered SEMS have a higher rate of migration and do not appear to have longer patency.[20]

Necessity for endoscopic sphincterotomy

Large-bore plastic stents can cause stent-induced pancreatitis.[21] Therefore, as SEMS placement is thought to cause pancreatitis because of occlusion of the pancreatic duct orifice, endoscopic sphincterotomy (ES) is more popular. One retrospective study showed that the frequency of post-ERCP pancreatitis (PEP) was significantly higher with placement of a SEMS than with a PS, although rates of PEP were similar when using covered and uncovered SEMS.[22] However, Banerjee et al. revealed that ES is not necessary during transpapillary biliary SEMS placement because there is no risk of pancreatitis and, instead, it may put the patient at increased risk for complications, including abdominal pain and post-ES bleeding.[23] However, that was a retrospective study and there is a possibility that an intact pancreatic duct, such as in distal bile duct cancer, may be more susceptible for SEMS placement-induced pancreatitis, apart from the head of the pancreas in pancreatic cancer, which usually has an obstructed pancreatic duct, suggesting a lower degree of pancreatitis after biliary SEMS placement. We have encountered fully covered SEMS placement-induced severe pancreatitis in a case of cholangiocarcinoma,[24] eventually resulting in death, although there was no fatal pancreatitis in the head of the pancreas. In addition to the histological type, we should compare the occurrence rate of pancreatitis between cases receiving fully covered and partially covered SEMS. Thus, prospective studies are warranted from the aspect of an intact or non-intact pancreatic duct.

Suprapapillary versus transpapillary stent placement

Placement of stents above an intact sphincter of Oddi might prevent migration of bacteria and deposition of organic material within the stent.[25] In terms of plastic stent placement in patients with malignant obstructive jaundice, one randomized trial by Pedersen et al. revealed that there was no significant difference in overall stent performance between suprapapillary and transpapillary stent placement, although more stents placed above the sphincter of Oddi migrated.[25] With regard to SEMS placement, one retrospective study suggested that transpapillary stent placement was the most significant factor for cholangitis after SEMS placement.[26] Thus, further prospective comparative studies are warranted.

Reintervention

Reintervention due to stent occlusion and stent misplacement is an inevitable possibility in biliary stenting. Of the two complications, stent occlusion is the most common problem. In terms of occluded plastic stents, stent exchange is relatively easy, but not for SEMS. An intervention for SEMS occlusion involves mechanical cleaning by a balloon catheter and the stent-in-stent procedure with plastic stents or additional SEMS. Interestingly, a recent systematic review of 10 retrospective studies revealed that the strategy of placing a plastic stent may be as effective as a second SEMS.[27]

Recently, a procedure whereby SEMS are removed and replaced by new SEMS has been developed as an alternative method for the management of SEMS occlusion (Table 4).[28-32] These data suggested that a new SEMS allows a longer stent patency than conventional occluded stent management (i.e. stent cleaning, additional placement of plastic stent or SEMS).[33] Furthermore, as an intervention in SEMS displacement, SEMS trimming by argon plasma coagulation (APC) has been used in cases of stent migration to the duodenum (Table 5).[32, 34-38]

Table 4. Outcomes of metal stent removal
AuthorNo. patientsDuration of stent placementTechnical success rate (%)Complications
UCUCUCUC
  1. *P < 0.05.

  2. C, covered metal stent; d, day; mo, month; U, uncovered metal stent; w, week.

Kahaleh et al.[28]4141 w–16 mo7510000
Familiari et al.[29]13297.5 mo3892*00
Shin et al.[30]822121 d–130 d (mean)08600
Kahaleh et al.[31]0654 moNA10000
Ishii et al.[32]11832 d–280 d07800
Table 5. Outcome of metal stent trimming
AuthorNo. patientsStentTechnical success rate (%)Complications (%)
  1. C, covered metal stent; SEMS, self-expandable metallic stent; U, uncovered metal stent.

Demarquay et al.[34]3Wallstent1000
Vanbiervliet et al.[35]24

Wallstent (23)

C-Wallstent (1)

Wallstent 96

C-Wallstent 100

0
Guda and Freeman[36]2

Wallstent (1)

C-Wallstent (1)

Wallstent 100

C-Wallstent 100

0
Rerknimitr et al.[37]2

Wallstent (1)

C-Wallstent (1)

Wallstent 100

C-Wallstent 100

0
Christiaens et al.[38]2U-SEMS (nitinol)1000
Ishii et al.[32]8

Wallstent (1)

C-Wallstent (3)

U-SEMS (nitinol) (4)

1000

Hilar Bile Duct Strictures

  1. Top of page
  2. Abstract
  3. Introduction
  4. Strategy of Biliary Stenting
  5. Distal Bile Duct Strictures
  6. Hilar Bile Duct Strictures
  7. Conclusions
  8. Acknowledgments
  9. Conflict of Interests
  10. References

Preprocedural evaluation

The management of hilar bile duct strictures is more difficult than that of distal bile duct strictures because of the diverse nature of the hilar bile ducts. Freeman and Overby advocated that computed tomography (CT) and magnetic resonance cholangiopancreatography (MRCP) are useful for preprocedural planning to evaluate and manage hilar obstruction for targeted SEMS placement.[39] Recently, Vienne et al. reported that a pre-endoscopic retrograde cholangiopancreatography (ERCP) assessment of hepatic volume distribution on cross-sectional imaging by CT may optimize endoscopic procedures because draining more than 50% of the liver volume seems to be an important predictor of drainage effectiveness in malignant, especially Bismuth III, hilar biliary strictures.[40]

Plastic stents versus SEMS

Two RCT[41, 42] and one prospective multicenter study[43] revealed that metal stent insertion for palliation of hilar malignancies seems to be superior to plastic stents in terms of longer stent patency, fewer complications, lower need for reintervention and better cost-effectiveness (Table 6). Based on these results, SEMS seem to be ideal stents for the therapy of hilar biliary strictures compared with plastic stents.

Table 6. Comparison between PS and SEMS for palliation of malignant hilar biliary obstruction
AuthorStudy designNo. patientsTechnical success (%)Early stent dysfunction (%)Late stent dysfunction (%)No. reinterventions
PSSEMSPSSEMSPSSEMSPSSEMSPSSEMS
  1. *P < 0.05.

  2. †50% patency (days).

  3. ‡6-month patency.

  4. NA, not available; P, prospective multicenter cohort study; PS, plastic stent; RCT, randomized controlled trial; SEMS, self-expandable metallic stent.

Wagner et al.[41]RCT9118910022050182.4*0.4
Perdue et al.[43]P28 (bilateral: 4)34 (bilateral: 5)859739*12NANANANA
Mukai et al.[42]RCT30 (bilateral: 15)30 (bilateral: 16)100100112 d359 d81*201.80.63

Unilateral versus bilateral stent placement

The selection of unilateral versus bilateral stent placement is still under debate because the management of Bismuth type III and IV hilar biliary strictures[44] is very complicated. Two retrospective studies[45, 46] have shown that bilateral SEMS were more effective than unilateral SEMS in terms of survival and cumulative stent patency. However, two RCT[42, 47] revealed that there were no significant differences between the two groups in terms of the rate of successful drainage, complications, and mortality (Table 7). Furthermore, reintervention for stent dysfunction was more complicated in bilateral stenting than in unilateral stenting.[42] Based on these data, DePalma et al. advocated that insertion of more than one stent would not appear justified as a routine procedure in patients with biliary bifurcation tumors.[47] A recent retrospective review of a large number of patients[48] suggested that bilateral SEMS placement offered the best results in terms of cumulative stent patency and reduced the need for repeat endoscopic biliary drainage resulting from stent occlusion, but only in Bismuth type II patients.

Table 7. RCT comparing unilateral and bilateral stent placement of PS and SEMS for palliation of malignant hilar biliary obstruction
AuthorStentStudy designNo. patientsTechnical success rate (%)Clinical success rate (%)Early complicationsLate complications (%)Successful reintervention rate (%)
  1. *P < 0.05.

  2. †Initial stent occlusion rate.

  3. NA, not available; PS, plastic stent; RCT, randomized controlled trials; SEMS, self-expandable metallic stent.

De Palma et al.[47]SEMSUnilateral7989*81*19%*40NA
Bilateral (side by side)78777327%39NA
Mukai et al.[42]SEMSUnilateral14100NA29%NA100
Bilateral (stent in stent)16100NA50%NA63
PSUnilateral15100NA67%NA100
Bilateral15100NA73%NA73

Side-by-side versus stent-in-stent placement

Bilateral SEMS placement includes side-by-side and stent-in-stent placement. Although the recent development of dedicated SEMS for hilar biliary strictures (e.g. Y-configured shape [Fig. 3]), the large-mesh and small-caliber 5-Fr delivery system has permitted the relatively high success rate of SEMS placement, regardless of the fact that side-by-side or stent-in-stent transpapillary bilateral SEMS placement is always more technically challenging than unilateral stenting. The selection of side-by-side versus stent-in-stent placement using metal stents for hilar biliary strictures is under debate. A recent retrospective study[49] showed that the incidence of complications is higher for side-by-side placement than for stent-in-stent deployment in bilateral metal stenting. In terms of cumulative stent patency, side-by-side deployment tends to be more effective than stent-in-stent deployment. Since, at present, there are few data, further prospective comparative studies are warranted.

figure

Figure 3. Stent in stent placement for hilar biliary strictures. (a) Y-configured metal stent (Large-D-cell type; Taewoong Medical, Seoul, Korea). (b) X-ray imaging of Y-configured metal stent (BONASTENT; Standard Sci-Tech, Inc., Seoul, Korea).

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Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Strategy of Biliary Stenting
  5. Distal Bile Duct Strictures
  6. Hilar Bile Duct Strictures
  7. Conclusions
  8. Acknowledgments
  9. Conflict of Interests
  10. References

In the present review, we described the current status of biliary stenting in patients with unresectable malignant biliary strictures. For now, SEMS is the most ideal biliary stent both for distal and hilar biliary strictures, although in terms of distal biliary strictures, the selection of covered or uncovered SEMS, suprapapillary or transpapillary stent placement, side-by-side or stent-in-stent placement, unilateral or bilateral stent placement and the necessity for sphincterotomy are still being debated. Therefore, further high-quality RCT to determine the suitability of these stent types and procedures are warranted.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Strategy of Biliary Stenting
  5. Distal Bile Duct Strictures
  6. Hilar Bile Duct Strictures
  7. Conclusions
  8. Acknowledgments
  9. Conflict of Interests
  10. References

The authors are indebted to Associate Professor Edward F. Barroga and Professor J. Patrick Barron, Chairman of the Department of International Medical Communications of Tokyo Medical University, for their editorial review of this manuscript.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Strategy of Biliary Stenting
  5. Distal Bile Duct Strictures
  6. Hilar Bile Duct Strictures
  7. Conclusions
  8. Acknowledgments
  9. Conflict of Interests
  10. References
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