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Temporary placement of covered self-expandable metal stents in benign biliary strictures: a new paradigm? (with video)
ORIGINAL ARTICLE: Clinical Endoscopy
Temporary placement of covered self-expandable metal stents in benign biliary strictures: a new paradigm? (with video) Michel Kahaleh, MD, FASGE, Brian Behm, MD, Bridger W. Clarke, MD, Andrew Brock, MD, Vanessa M. Shami, MD, Sarah A. De La Rue, PhD, Vinay Sundaram, MD, Jeffrey Tokar, MD, Reid B. Adams, MD, Paul Yeaton, MD Charlottesville, Virginia, USA
Background: Benign biliary strictures (BBS) are usually managed with plastic stents, whereas placement of uncovered metallic stents has been associated with failure related to mucosal hyperplasia. Objective: We analyzed the efficacy and safety of temporary placement of a covered self-expanding metal stent (CSEMS) in BBS. Design: Patients with BBS received temporary placement of CSEMSs until adequate drainage was achieved; confirmed by resolution of symptoms, normalization of liver function tests, and imaging. Setting: Tertiary-care center with long-standing experience with CSEMSs. Patients: Seventy-nine patients with BBS secondary to chronic pancreatitis (32), calculi (24), liver transplant (16), postoperative biliary repair (3), autoimmune pancreatitis (3), and primary sclerosing cholangitis (1). Intervention: ERCP with temporary CSEMS placement. Removal of CSEMSs was performed with a snare or a rat-tooth forceps. Main Outcome Measurements: End points were efficacy, morbidity, and clinical response. Results: CSEMSs were removed from 65 patients. Resolution of the BBS was confirmed in 59 of 65 patients (90%) after a median follow-up of 12 months after removal (range 3-26 months). If patients who were lost to follow-up, developed cancer, or expired were considered failures, then an intent-to-treat global success rate of 59 of 79 (75%) was obtained. Complications associated with placement included 3 post-ERCP pancreatitis (4%), 1 postsphincterotomy bleed (1%), and 2 pain that required CSEMS removal (2%). In 11 patients (14%), the CSEMS migrated. In 1 patient, CSEMS removal was complicated by a bile leak that was successfully managed with plastic stents. Limitation: Pilot study from a single center. Conclusions: Temporary CSEMS placement in patients with BBS offers a potential alternative to surgery. (Gastrointest Endosc 2008;67:446-54.)
Benign biliary strictures (BBS) can result from chronic pancreatitis, biliary calculi, trauma, sclerosing cholangitis, surgery, and rare cholangiopathies.1 Biliary strictures may lead to pain, jaundice, cholangitis, and secondary biliary cirrhosis.2 Given this morbid natural history, biliary decompression is crucial. Current decompressive options include hepaticojejunostomy, percutaneous dilation, or
Copyright ª 2008 by the American Society for Gastrointestinal Endoscopy 0016-5107/$32.00 doi:10.1016/j.gie.2007.06.057
endoscopic balloon dilation and stent placement. Although balloon dilation alone has been shown to be inferior,3 debate exists regarding whether endoscopic stent placement is equivalent to surgery. Although surgery has the theoretical advantage of being definitive,4 endoscopic stent placement has gained acceptance as an initial treatment because of its simplicity and low morbidity and mortality. Compared with surgery, stent placement has lower rates of stricture recurrence,5-7 and endoscopic treatment preserves the option of surgery if repeated endoscopic attempts fail.8 Current data favor the use of plastic stents in BBS.8-12 Although uncovered self-expanding metal stents (SEMSs)
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Abbreviations: ALK, alkaline phosphatase; ALT, alanine aminotransferase; BBS, benign biliary strictures; CSEMS, covered self-expanding metal stent; LFT, liver function test; SEMS, self-expanding metal stent.
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were shown to have a longer duration of patency than plastic stents in malignant strictures,13-17 their use in benign biliary disease was associated with long-term failure related to mucosal hyperplasia7 and the lack of removability. Covered SEMSs (CSEMSs) have been shown to remain patent longer than uncovered SEMSs18,19 and have the added advantage of being removable by endoscopy in the event of malfunction.20-22 These observations prompted our prospective evaluation of BBS management by using CSEMSs. We report our experience treating patients with BBS with temporary placement of CSEMSs since 2001.23
PATIENTS AND METHODS
Stents in benign biliary strictures
Capsule Summary What is already known on this topic d
Uncovered self-expanding metal stents (SEMSs) have longer durations of patency than plastic stents in malignant strictures, but their use in benign biliary strictures (BBS) is associated with long-term failure.
What this study adds to our knowledge d
In a single-center pilot study, 59 of 65 patients had resolution of BBS with placement of covered SEMSs until adequate drainage was achieved, resulting in a success rate of 75%.
Patients Between December 2001 and December 2005, 79 patients (54 men), with a mean age of 55 15 years, who had benign biliary obstruction, were enrolled in a prospective study for CSEMS placement (Table 1). Patients were then followed prospectively in the clinic with liver function tests (LFTs) every 3 months until death or stent dysfunction, or as clinically indicated. Patients in whom biliary decompression was confirmed by resolution of symptoms, normalization of LFTs, and imaging underwent CSEMS removal. The clinical response to therapy, procedure-related morbidity, and symptoms were recorded. Success was defined as persistent clinical resolution of the stricture without the need for repeat stent placement. The study was approved by our institutional review board. All patients provided written consent for their procedures.
CSEMS insertion, deployment, and removal All CSEMSs placed were partially covered with Permalume (Microvasive Endoscopy, Boston Scientific Corp, Natick, Mass), 10 mm in diameter, and had a 1-cm uncovered portion on both the proximal and distal stent ends. After biliary sphincterotomy, the length of each stricture was determined (Fig. 1) and the origin of the cystic-duct insertion was noted in patients with an intact gallbladder. The proximal CSEMS delivery system was advanced above the stricture over a guidewire where the CSEMS (40, 60, or 80 mm) was partially deployed and positioned within the stricture before complete deployment (Fig. 2). When the gallbladder was still present, CSEMSs were placed below the cystic-duct insertion. Removal was performed by using the snare (Video 1, available online at www.giejournal.org) or rat-tooth technique.23 All procedures were performed by 1 of 2 dedicated pancreaticobiliary endoscopists (M.K. or P.Y.).
echoendoscopes (Olympus America, Center Valley, Pa) whenever the etiology of the stricture was unclear to rule out malignancy.
Definition of events Successful CSEMS placement was defined as biliary decompression after CSEMS deployment, with relief of jaundice, pruritus, and/or cholestasis. Complications were stratified as early (occurring %30 days of CSEMS placement) and late (occurring O30 days after CSEMS placement).
Statistics The primary end point analyzed was resolution of the biliary stricture after CSEMS removal. The mean levels of alanine aminotransferase (ALT) (reference range !55 IU/L), alkaline phosphatase (ALK) (40-150 IU/L), and total bilirubin (0.3-1.2 mg %) before and after treatment were tested for significance by using the t test. A multivariate logistical regression analysis of factors potentially predictive of success (eg, patient age, time in place, SEMS length, and etiology) was performed. The level of significance was set at P!.05 in the statistical analyses.
RESULTS Early complications (%30 days) CSEMSs were successfully placed in all patients. Early complications related to CSEMS insertion included 2 cases of mild post-ERCP pancreatitis managed conservatively, 1 case of pancreatitis with infected pseudocyst that required CSEMS removal and transpapillary drainage, and 1 case of postsphincterotomy bleeding that required hemoclip placement. In 2 patients, abdominal pain after CSEMS placement necessitated their removal.
Imaging Patients were imaged by using CT, magnetic resonance, and/or EUS. EUS was performed with Olympus instruments, including GF-UCT140 and/or GF-UM160
Long-term complications (O30 days)
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Two CSEMSs migrated distally and became lodged in the duodenum, with persistent stricture; these were
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TABLE 1. Global study population characteristics Characteristics
No.
No. patients
79
Sex (male/female) Mean age (y)
54/25 55 (range 21-93)
Etiology of BBS Chronic pancreatitis
32
Biliary calculi
24
Liver transplant
16
Inflammatory
4
Surgical
3
CSEMS length 40 mm
37
60 mm
34
80 mm
8
Mean (SD) bilirubin (mg/dL)
3.9 4.5 (range 0.2-20)
Mean (SD) ALK (IU/L)
406 419 (range 50-931)
Mean (SD) ALT (IU/L)
85 96 (range 102-526)
SD, Standard deviation.
Figure 1. Anastomotic stricture after liver transplant (patient A).
removed endoscopically. In 3 patients, spontaneous migration and expulsion of the CSEMS was observed, with resolution of the stricture; these were not counted as complications at the end of the study. In 6 cases, proximal migration resulted in tissue ingrowth in the distal uncovered portion of the stent that required balloon dilation before extraction. In another patient, CSEMS removal was complicated by a bile leak related to a malpositioned dilating balloon placed above the metal stent and resulted in a sudden rupture. This was successfully managed with plastic stents. Two patients developed cholecystitis in the setting of cholelithiasis: 1 before CSEMS removal and 1 at 10 months after CSEMS removal, and both underwent cholecystectomy.
CSEMSs were left in place for a median time of 4 months (range 1-28 months) in 65 patients and were removed once successful treatment was confirmed by symptom resolution, LFT normalization (Figs. 3 to 5) (P Z .001), and repeat imaging. Patients were followed after CSEMS removal for a median of 12 months (range 3-26 months). Three patients developed a stricture in the uncovered proximal portion, 3 failed primary therapy, and 2 developed duodenal edema that prevented CSEMS removal, resulting in a success rate of 59 of 65 (90%). When a breakdown by
etiology of stricture was performed (Fig. 6), 17 of 22 patients (77%) with chronic pancreatitis, 15 of 16 patient (94%) with anastomotic stricture after liver transplant, and 27 of 27 patients (100%) with BBS from other etiology responded to treatment at the end of the study. An intent-to-treat global success rate of 59 of 79 (75%) was computed if patients who were lost to follow-up, developed duodenal edema that prevented CSEMS removal, developed cancer, or expired were considered failures. Logistical regression analysis failed to identify any factor predictive of success (eg, patient age, time in place, CSEMS length, and etiology). Of the 14 patients who did not undergo CSEMS removal during the study period, 3 were lost to followup, 1 developed hepatocellular carcinoma; 3 developed pancreatic cancer; 2 developed duodenal inflammation, which prevented access to the second portion for CSEMS removal; and 5 died from unrelated causes (1 urinary sepsis, 1 decompensated alcoholic cirrhosis, and 3 sudden deaths related to coronary heart disease). The 2 patients with duodenal edema received enteral feeding through a PEG jejunostomy until the inflammation completely resolved. The 6 patients who failed CSEMS treatment received plastic stents (4) or repeat CSEMS placement (2).
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Reinterventions and final results
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Figure 4. ALK level before CSEMS placement and after CSEMS removal.
Figure 2. Placement of a CSEMS (10 80 mm) across the stricture with excellent biliary decompression (patient A).
Figure 5. ALT level before CSEMS placement and after CSEMS removal.
Plastic stents have frequently been used in the management of patients with BBS.9-12,24 Plastic stents appear to
provide a long term resolution in a minority of patients with strictures caused by chronic pancreatitis,6,25 whereas patients with postoperative injury require repeat interventions over a long time period7 or an approach that maximizes the number of large-diameter plastic stents placed.11 Indeed, plastic stents have limited patency rates, becoming occluded within 3 to 6 months, requiring frequent replacement and increasing numbers of stents.11 The major factor that limits plastic-stent patency is the formation of a bacterial biofilm that leads to deconjugation of bile-acid salts, with sludge and stone formation related to the stent.26-28 Efforts to prolong plastic-stent patency by changing stent design29,30 by administering ursodeoxycholic acid, aspirin, or antibiotics27,29,31,32 have had little impact on patency rates in vivo. Recent studies confirmed the implication of duodenobiliary reflux,33 with dietary fiber forming a filter within the stent.34 This may explain why large-diameter stents have improved
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Figure 3. Total bilirubin (TB) level before CSEMS placement and after CSEMS removal.
DISCUSSION
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Figure 6. Long-term follow-up of the 79 patients who received CSEMSs with final long-term resolution provided. (CP, chronic pancreatitis; BC, biliary calculi; OLT, orthotopic liver transplant; INFL, inflammatory; SURG, surgical; Neo, neoplasia; LTF, lost to follow-up, DUOD INFL, duodenal inflammation).
TABLE 2. Series reporting CSEMS placement for BBS
Study
No. patients/ no. stents Etiology
Stent type
Time to removal, median (range) 5.25 mo (3-6 mo)
Bruno et al,46 2005
4/4
CP
Fully covered
Tringali et al,53 2005
6/6
CP
PCM
N/A
Cantu, et al,48 2005
14/14
CP
PCM
3/4
OTL
Fully covered
Kuo et al,47 2006
Reason for removal (no. of stents)
Resolution
Complications (no. of patients)
Per operator (4)
75% at removal
Prox migration (1)
N/A
2 CSEMS patent at 35-mo fup
Not reported
21 mo (18-33 mo)
Hyperplasia (5), migration (2), not removed (7)
37.5% at 30-mo fup
Cholestasis (7), cholangitis (5), duod migration (2), cholecystitis (1)
32 d (0-49 d)
Misplacement (1); per operator (2)
100% at removal
Septicemia (1), misplacement (1)
CP, Chronic pancreatitis; Prox, proximal; PCM, partially covered metal; N/A, not available; fup, follow-up; duod, duodenal; OTL, orthotopic liver transplantation.
patency rates compared with smaller-diameter stents. The diameter of plastic stents is limited by the accessory channel dimension, and this, in part, led to the development of SEMSs. For more than a decade, SEMSs have been the accepted therapy for palliation of malignant biliary obstruction,13-16,35 but their role in benign biliary disease remains controversial. Uncovered SEMS placement for BBS has been reported,7,36,37 but its acceptance has been limited by the observation of benign hyperplasia that
compromised patency.38 Despite their limitations, there is some support for the use of uncovered SEMSs in the management of refractory benign strictures.39 Not surprisingly, studies that compared surgery with uncovered SEMSs demonstrated that surgery is superior, primarily because of issues of patency and poor removability with uncovered SEMSs.40 Some investigators argue that the use of uncovered SEMSs in BBS should be avoided in patients with a life expectancy longer than 2 years.41
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Stents in benign biliary strictures
Figure 7. Distal biliary stricture related to chronic pancreatitis (patient C).
In an attempt to improve the durability of patency, coverings were proposed for SEMSs,42,43 with good effect. Their improved patency, compared with uncovered SEMSs,19 combined with the theoretical ability to remove CSEMSs, led to studies that assessed their utility in the setting of benign distal biliary strictures23,44 (Table 2). Trentino et al45 described placement of a CSEMS and its removal 6 months later in a patient with an anastomotic stricture after orthotopic liver transplantation. A study that evaluated 4 patients with chronic pancreatitis–associated biliary strictures found that removal of a fully covered CSEMS (Hanaro endoprosthesis; M.I. Tech Corporation, Seoul, South Korea) was feasible up to 6 months after placement and found resolution of biliary strictures in 3 of 4 patients after removal.46 In a recent series by Kuo et al,47 the investigators describe percutaneous placement of a CSEMS (Viabil; W.L. Gore and Associates, Flagstaff, Ariz) in 3 patients with strictures after orthotopic liver transplantation, and 1 stricture of unknown etiology. One patient developed a biliary-hepatic arterial fistula in the contralateral side to the stent placement, which was treated successfully with coil embolization; and 1 patient developed infection, which was treated conservatively. All CSEMSs were removed percutaneously except 1 removed by combined antegrade and retrograde approach. Interestingly, in that study, there were no episodes of CSEMS migration, and all stents remained patent for the duration of placement. Cantu et al48 published a series that evaluated CSEMSs in BBS that resulted from chronic pancreatitis; 14 patients underwent partially covered Wallstent (Boston Scientific, Natick, Mass) placement with no intention to remove. All stents remained patent 18 months after placement, but, in the ensuing period of observation, with a median follow-up of 22 months, half developed stent dysfunction
secondary to tissue hyperplasia (5 patients) and stent migration (2 patients). One patient developed cholecystitis, despite CSEMS deployment below the cystic-duct insertion. By design, all CSEMSs were left in place until the patients developed symptoms of stent dysfunction. Only 1 migrated CSEMS was removed; resolution of the biliary stricture was observed. In our study, CSEMSs were left in place until the study criteria for success were met. Sixty-five patients had CSEMSs removed after a median of 4 months; 59 of these had stricture resolution, without the need for further biliary intervention (Figs. 7 to 9). This provides a success rate of 59 of 65 (90%), because 2 patients developed duodenal edema, which prevented CSEMS removal. If the patients who were lost to follow-up, developed duodenal edema, cancer, or expired were considered failures, then an intent-to-treat global success rate of 59 of 79 patients (75%) was obtained. This compares
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Figure 8. Placement of a CSEMS (10 60 mm) across the stricture in regard of the pancreatic stent placed (patient C).
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Figure 10. Normalization of the common hepatic duct enlargement 3 months later (patient B).
Figure 9. Enlargement of the common hepatic duct after CSEMS removal in a patient treated for an anastomotic stricture after liver transplant (patient B).
favorably with the long-term success rate reported in patients with chronic pancreatitis or after surgical strictures, estimated at 35%49,50 and 80%,51,52 respectively. Based on our experience, removal of Wallstents beyond 6 months is feasible but more challenging, potentially requiring grasping the interior of the CSEMS with a rat-tooth forceps. Another interesting observation is related to the temporary enlargement of the distal bile duct after CSEMS removal. This seems to resolve over time (Figs. 9 and 10). Early complications occurred in 8% (6 patients), half of them related to the stent. Late complication occurred in 14% (11 patients), 73% of them (8 patients) related to the stent. Eleven patients had distal CSEMS migration, 7 of whom had short (40 mm) CSEMSs; although the use of 60- and 80-mm stents appeared to decrease the risk, this observation was not statistically supported (P Z .252). CSEMS placement is associated with pancreatitis.18,19 In our study, 2 cases of pancreatitis were mild, which required only observation. One patient who presented 452 GASTROINTESTINAL ENDOSCOPY Volume 67, No. 3 : 2008
with pancreatitis complicated by pancreatic-duct disruption underwent CSEMS placement and subsequently developed an infected pseudocyst. The collection resolved with endoscopic decompression. This was the only patient in whom biliary sphincterotomy did not prevent postERCP pancreatitis. In most cases of chronic pancreatitis, stents were placed, in the same session, in ductal strictures that involved both pancreatic and biliary ducts, with the distal end of the pancreatic stent protruding beyond the CSEMS (Figs. 7 and 8). In conclusion, CSEMSs successfully treated the majority of patients with BBS, with infrequent recurrence after removal and with complication rates within an acceptable range. We do not recommend leaving Wallstents in place beyond 6 months. With the arrival of additional CSEMSs, cost can be anticipated to decrease, making this an even more attractive option for benign diseases. It remains to be demonstrated that CSEMS removability can be improved, migration decreased, and final success improved.
ACKNOWLEDGMENTS We thank Penny Bashlor, RN, and Kristi Ellen, RN, for their critical contribution in the clinical follow-up of the patients enrolled in this study. www.giejournal.org
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Stents in benign biliary strictures
1. Lillemoe KD, Melton GB, Cameron JL, et al. Postoperative bile duct strictures: management and outcome in the 1990s. Ann Surg 2000;232:430-41. 2. Warshaw AL, Schapiro RH, Ferrucci JT Jr, et al. Persistent obstructive jaundice, cholangitis, and biliary cirrhosis due to common bile duct stenosis in chronic pancreatitis. Gastroenterology 1976;70:562-7. 3. Pitt HA, Kaufman SL, Coleman J, et al. Benign postoperative biliary strictures. Operate or dilate? Ann Surg 1989;210:417-25; discussion 426-7. 4. Nealon WH, Urrutia F. Long-term follow-up after bilioenteric anastomosis for benign bile duct stricture. Ann Surg 1996;223:639-45; discussion 645-8. 5. Davids PH, Tanka AK, Rauws EA, et al. Benign biliary strictures. Surgery or endoscopy? Ann Surg 1993;217:237-43. 6. Smits ME, Rauws EA, van Gulik TM, et al. Long-term results of endoscopic stenting and surgical drainage for biliary stricture due to chronic pancreatitis. Br J Surg 1996;83:764-8. 7. Dumonceau JM, Deviere J, Delhaye M, et al. Plastic and metal stents for postoperative benign bile duct strictures: the best and the worst. Gastrointest Endosc 1998;47:8-17. 8. Frattaroli FM, Reggio D, Guadalaxara A, et al. Benign biliary strictures: a review of 21 years of experience. J Am Coll Surg 1996;183:506-13. 9. Berkelhammer C, Kortan P, Haber GB. Endoscopic biliary prostheses as treatment for benign postoperative bile duct strictures. Gastrointest Endosc 1989;35:95-101. 10. Draganov P, Hoffman B, Marsh W, et al. Long-term outcome in patients with benign biliary strictures treated endoscopically with multiple stents. Gastrointest Endosc 2002;55:680-6. 11. Costamagna G, Pandolfi M, Mutignani M, et al. Long-term results of endoscopic management of postoperative bile duct strictures with increasing numbers of stents. Gastrointest Endosc 2001;54:162-8. 12. Davids PH, Rauws EA, Coene PP, et al. Endoscopic stenting for postoperative biliary strictures. Gastrointest Endosc 1992;38:12-8. 13. Davids PH, Groen AK, Rauws EA, et al. Randomised trial of self-expanding metal stents versus polyethylene stents for distal malignant biliary obstruction. Lancet 1992;340:1488-92. 14. Kaassis M, Boyer J, Dumas R, et al. Plastic or metal stents for malignant stricture of the common bile duct? Results of a randomized prospective study. Gastrointest Endosc 2003;57:178-82. 15. Knyrim K, Wagner HJ, Pausch J, et al. A prospective, randomized, controlled trial of metal stents for malignant obstruction of the common bile duct. Endoscopy 1993;25:207-12. 16. Wagner HJ, Knyrim K, Vakil N, et al. Plastic endoprostheses versus metal stents in the palliative treatment of malignant hilar biliary obstruction. A prospective and randomized trial. Endoscopy 1993;25: 213-8. 17. Katsinelos P, Paikos D, Kountouras J, et al. Tannenbaum and metal stents in the palliative treatment of malignant distal bile duct obstruction: a comparative study of patency and cost effectiveness. Surg Endosc 2006;20:1587-93.
18. Bezzi M, Zolovkins A, Cantisani V, et al. New ePTFE/FEP-covered stent in the palliative treatment of malignant biliary obstruction. J Vasc Interv Radiol 2002;13:581-9. 19. Isayama H, Komatsu Y, Tsujino T, et al. A prospective randomised study of ‘‘covered’’ versus ‘‘uncovered’’ diamond stents for the management of distal malignant biliary obstruction. Gut 2004;53:729-34. 20. Wamsteker EJ, Elta GH. Migration of covered biliary self-expanding metallic stents in two patients with malignant biliary obstruction. Gastrointest Endosc 2003;58:792-3. 21. Matsushita M, Takakuwa H, Nishio A, et al. Open-biopsy-forceps technique for endoscopic removal of distally migrated and impacted biliary metallic stents. Gastrointest Endosc 2003;58:924-7. 22. Minami A, Fujita R. A new technique for removal of bile duct stones with an expandable metallic stent. Gastrointest Endosc 2003;57:945-8. 23. Kahaleh M, Tokar J, Le T, et al. Removal of self-expandable metallic Wallstents. Gastrointest Endosc 2004;60:640-4. 24. Huibregtse K, Katon RM, Tytgat GN. Endoscopic treatment of postoperative biliary strictures. Endoscopy 1986;18:133-7. 25. Barthet M, Bernard JP, Duval JL, et al. Biliary stenting in benign biliary stenosis complicating chronic calcifying pancreatitis. Endoscopy 1994;26:569-72. 26. Coene PP, Groen AK, Cheng J, et al. Clogging of biliary endoprostheses: a new perspective. Gut 1990;31:913-7. 27. Sung JY, Shaffer EA, Costerton JW. Antibacterial activity of bile salts against common biliary pathogens. Effects of hydrophobicity of the molecule and in the presence of phospholipids. Dig Dis Sci 1993;38:2104-12. 28. Leung JW, Ling TK, Kung JL, et al. The role of bacteria in the blockage of biliary stents. Gastrointest Endosc 1988;34:19-22. 29. England RE, Martin DF, Morris J, et al. A prospective randomised multicentre trial comparing 10 Fr Teflon Tannenbaum stents with 10 Fr polyethylene Cotton-Leung stents in patients with malignant common duct strictures. Gut 2000;46:395-400. 30. Costamagna G, Mutignani M, Rotondano G, et al. Hydrophilic hydromer-coated polyurethane stents versus uncoated stents in malignant biliary obstruction: a randomized trial. Gastrointest Endosc 2000;51: 8-11. 31. Libby ED, Leung JW. Ultrasmooth plastic to prevent stent clogging. Gastrointest Endosc 1994;40:386-7. 32. Ghosh S, Palmer KR. Prevention of biliary stent occlusion using cyclical antibiotics and ursodeoxycholic acid. Gut 1994;35:1757-9. 33. Weickert U, Venzke T, Konig J, et al. Why do bilioduodenal plastic stents become occluded? A clinical and pathological investigation on 100 consecutive patients. Endoscopy 2001;33:786-90. 34. van Berkel AM, van Marle J, Groen AK, et al. Mechanisms of biliary stent clogging: confocal laser scanning and scanning electron microscopy. Endoscopy 2005;37:729-34. 35. Prat F, Chapat O, Ducot B, et al. A randomized trial of endoscopic drainage methods for inoperable malignant strictures of the common bile duct. Gastrointest Endosc 1998;47:1-7. 36. Yamaguchi T, Ishihara T, Seza K, et al. Long-term outcome of endoscopic metallic stenting for benign biliary stenosis associated with chronic pancreatitis. World J Gastroenterol 2006;12:426-30. 37. Irving JD, Adam A, Dick R, et al. Gianturco expandable metallic biliary stents: results of a European clinical trial. Radiology 1989;172:321-6. 38. Wadhwa RP, Kozarek RA, France RE, et al. Use of self-expandable metallic stents in benign GI diseases. Gastrointest Endosc 2003;58:207-12. 39. Jeng KS, Sheen IS, Yang FS. Are expandable metallic stents better than conventional methods for treating difficult intrahepatic biliary strictures with recurrent hepatolithiasis? Arch Surg 1999;134:267-73. 40. Lopez RR Jr, Cosenza CA, Lois J, et al. Long-term results of metallic stents for benign biliary strictures. Arch Surg 2001;136:664-9. 41. Siriwardana HP, Siriwardena AK. Systematic appraisal of the role of metallic endobiliary stents in the treatment of benign bile duct stricture. Ann Surg 2005;242:10-9. 42. Shim CS, Lee YH, Cho YD, et al. Preliminary results of a new covered biliary metal stent for malignant biliary obstruction. Endoscopy 1998; 30:345-50.
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DISCLOSURES The following authors report that they have no disclosures relevant to this publication: B. Behm, B. W. Clarke, A. Brock, V. M. Shami, S. A. De La Rue, V. Sundaram, J. Tokar, R. B. Adams. The following authors have disclosed actual or potential conflicts: M. Kahaleh has received grant support from Boston Scientific, Alveolus, and Cook Medical. P. Yeaton has received grant support from Olympus and Alveolus.
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51. Bergman JJ, Burgemeister L, Bruno MJ, et al. Long-term follow-up after biliary stent placement for postoperative bile duct stenosis. Gastrointest Endosc 2001;54:154-61. 52. Alazmi WM, Fogel EL, Watkins JL, et al. Recurrence rate of anastomotic biliary strictures in patients who have had previous successful endoscopic therapy for anastomotic narrowing after orthotopic liver transplantation. Endoscopy 2006;38:571-4. 53. Tringali A, Di Matteo F, Iacopini F, et al. Common bile duct strictures due to chronic pancreatitis managed by self-expandable metal stents: results of a long term follow-up study [abstract]. Gastrointest Endosc 2005;61:AB220.
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Received November 9, 2006. Accepted June 25, 2007. Current affiliations: Digestive Health Center (M.K., B.B., B.W.C., A.B., V.M.S., S.D.L.R., V.S., J.T., P.Y.), the Department of Surgery (R.B.A.), University of Virginia Health System, Charlottesville, Virginia, USA. Presented at Digestive Disease Week, Chicago, Illinois, May 14-18, 2005, and Washington, DC, May 20-23, 2007 (Gastrointest Endosc 2005;61: AB208, Gastrointest Endosc 2007;65:AB123). Reprint requests: Michel Kahaleh, MD, Digestive Health Center Box 800708, University of Virginia Health System, Charlottesville, VA 22908-0708.
Temporary placement of covered self-expandable metal stents in benign biliary strictures: a new paradigm? (with video) Michel Kahaleh, MD, FASGE, Brian Behm, MD, Bridger W. Clarke, MD, Andrew Brock, MD, Vanessa M. Shami, MD, Sarah A. De La Rue, PhD, Vinay Sundaram, MD, Jeffrey Tokar, MD, Reid B. Adams, MD, Paul Yeaton, MD Charlottesville, Virginia, USA
Background: Benign biliary strictures (BBS) are usually managed with plastic stents, whereas placement of uncovered metallic stents has been associated with failure related to mucosal hyperplasia. Objective: We analyzed the efficacy and safety of temporary placement of a covered self-expanding metal stent (CSEMS) in BBS. Design: Patients with BBS received temporary placement of CSEMSs until adequate drainage was achieved; confirmed by resolution of symptoms, normalization of liver function tests, and imaging. Setting: Tertiary-care center with long-standing experience with CSEMSs. Patients: Seventy-nine patients with BBS secondary to chronic pancreatitis (32), calculi (24), liver transplant (16), postoperative biliary repair (3), autoimmune pancreatitis (3), and primary sclerosing cholangitis (1). Intervention: ERCP with temporary CSEMS placement. Removal of CSEMSs was performed with a snare or a rat-tooth forceps. Main Outcome Measurements: End points were efficacy, morbidity, and clinical response. Results: CSEMSs were removed from 65 patients. Resolution of the BBS was confirmed in 59 of 65 patients (90%) after a median follow-up of 12 months after removal (range 3-26 months). If patients who were lost to follow-up, developed cancer, or expired were considered failures, then an intent-to-treat global success rate of 59 of 79 (75%) was obtained. Complications associated with placement included 3 post-ERCP pancreatitis (4%), 1 postsphincterotomy bleed (1%), and 2 pain that required CSEMS removal (2%). In 11 patients (14%), the CSEMS migrated. In 1 patient, CSEMS removal was complicated by a bile leak that was successfully managed with plastic stents. Limitation: Pilot study from a single center. Conclusions: Temporary CSEMS placement in patients with BBS offers a potential alternative to surgery. (Gastrointest Endosc 2008;67:446-54.)
Benign biliary strictures (BBS) can result from chronic pancreatitis, biliary calculi, trauma, sclerosing cholangitis, surgery, and rare cholangiopathies.1 Biliary strictures may lead to pain, jaundice, cholangitis, and secondary biliary cirrhosis.2 Given this morbid natural history, biliary decompression is crucial. Current decompressive options include hepaticojejunostomy, percutaneous dilation, or
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endoscopic balloon dilation and stent placement. Although balloon dilation alone has been shown to be inferior,3 debate exists regarding whether endoscopic stent placement is equivalent to surgery. Although surgery has the theoretical advantage of being definitive,4 endoscopic stent placement has gained acceptance as an initial treatment because of its simplicity and low morbidity and mortality. Compared with surgery, stent placement has lower rates of stricture recurrence,5-7 and endoscopic treatment preserves the option of surgery if repeated endoscopic attempts fail.8 Current data favor the use of plastic stents in BBS.8-12 Although uncovered self-expanding metal stents (SEMSs)
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Abbreviations: ALK, alkaline phosphatase; ALT, alanine aminotransferase; BBS, benign biliary strictures; CSEMS, covered self-expanding metal stent; LFT, liver function test; SEMS, self-expanding metal stent.
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were shown to have a longer duration of patency than plastic stents in malignant strictures,13-17 their use in benign biliary disease was associated with long-term failure related to mucosal hyperplasia7 and the lack of removability. Covered SEMSs (CSEMSs) have been shown to remain patent longer than uncovered SEMSs18,19 and have the added advantage of being removable by endoscopy in the event of malfunction.20-22 These observations prompted our prospective evaluation of BBS management by using CSEMSs. We report our experience treating patients with BBS with temporary placement of CSEMSs since 2001.23
PATIENTS AND METHODS
Stents in benign biliary strictures
Capsule Summary What is already known on this topic d
Uncovered self-expanding metal stents (SEMSs) have longer durations of patency than plastic stents in malignant strictures, but their use in benign biliary strictures (BBS) is associated with long-term failure.
What this study adds to our knowledge d
In a single-center pilot study, 59 of 65 patients had resolution of BBS with placement of covered SEMSs until adequate drainage was achieved, resulting in a success rate of 75%.
Patients Between December 2001 and December 2005, 79 patients (54 men), with a mean age of 55 15 years, who had benign biliary obstruction, were enrolled in a prospective study for CSEMS placement (Table 1). Patients were then followed prospectively in the clinic with liver function tests (LFTs) every 3 months until death or stent dysfunction, or as clinically indicated. Patients in whom biliary decompression was confirmed by resolution of symptoms, normalization of LFTs, and imaging underwent CSEMS removal. The clinical response to therapy, procedure-related morbidity, and symptoms were recorded. Success was defined as persistent clinical resolution of the stricture without the need for repeat stent placement. The study was approved by our institutional review board. All patients provided written consent for their procedures.
CSEMS insertion, deployment, and removal All CSEMSs placed were partially covered with Permalume (Microvasive Endoscopy, Boston Scientific Corp, Natick, Mass), 10 mm in diameter, and had a 1-cm uncovered portion on both the proximal and distal stent ends. After biliary sphincterotomy, the length of each stricture was determined (Fig. 1) and the origin of the cystic-duct insertion was noted in patients with an intact gallbladder. The proximal CSEMS delivery system was advanced above the stricture over a guidewire where the CSEMS (40, 60, or 80 mm) was partially deployed and positioned within the stricture before complete deployment (Fig. 2). When the gallbladder was still present, CSEMSs were placed below the cystic-duct insertion. Removal was performed by using the snare (Video 1, available online at www.giejournal.org) or rat-tooth technique.23 All procedures were performed by 1 of 2 dedicated pancreaticobiliary endoscopists (M.K. or P.Y.).
echoendoscopes (Olympus America, Center Valley, Pa) whenever the etiology of the stricture was unclear to rule out malignancy.
Definition of events Successful CSEMS placement was defined as biliary decompression after CSEMS deployment, with relief of jaundice, pruritus, and/or cholestasis. Complications were stratified as early (occurring %30 days of CSEMS placement) and late (occurring O30 days after CSEMS placement).
Statistics The primary end point analyzed was resolution of the biliary stricture after CSEMS removal. The mean levels of alanine aminotransferase (ALT) (reference range !55 IU/L), alkaline phosphatase (ALK) (40-150 IU/L), and total bilirubin (0.3-1.2 mg %) before and after treatment were tested for significance by using the t test. A multivariate logistical regression analysis of factors potentially predictive of success (eg, patient age, time in place, SEMS length, and etiology) was performed. The level of significance was set at P!.05 in the statistical analyses.
RESULTS Early complications (%30 days) CSEMSs were successfully placed in all patients. Early complications related to CSEMS insertion included 2 cases of mild post-ERCP pancreatitis managed conservatively, 1 case of pancreatitis with infected pseudocyst that required CSEMS removal and transpapillary drainage, and 1 case of postsphincterotomy bleeding that required hemoclip placement. In 2 patients, abdominal pain after CSEMS placement necessitated their removal.
Imaging Patients were imaged by using CT, magnetic resonance, and/or EUS. EUS was performed with Olympus instruments, including GF-UCT140 and/or GF-UM160
Long-term complications (O30 days)
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Two CSEMSs migrated distally and became lodged in the duodenum, with persistent stricture; these were
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TABLE 1. Global study population characteristics Characteristics
No.
No. patients
79
Sex (male/female) Mean age (y)
54/25 55 (range 21-93)
Etiology of BBS Chronic pancreatitis
32
Biliary calculi
24
Liver transplant
16
Inflammatory
4
Surgical
3
CSEMS length 40 mm
37
60 mm
34
80 mm
8
Mean (SD) bilirubin (mg/dL)
3.9 4.5 (range 0.2-20)
Mean (SD) ALK (IU/L)
406 419 (range 50-931)
Mean (SD) ALT (IU/L)
85 96 (range 102-526)
SD, Standard deviation.
Figure 1. Anastomotic stricture after liver transplant (patient A).
removed endoscopically. In 3 patients, spontaneous migration and expulsion of the CSEMS was observed, with resolution of the stricture; these were not counted as complications at the end of the study. In 6 cases, proximal migration resulted in tissue ingrowth in the distal uncovered portion of the stent that required balloon dilation before extraction. In another patient, CSEMS removal was complicated by a bile leak related to a malpositioned dilating balloon placed above the metal stent and resulted in a sudden rupture. This was successfully managed with plastic stents. Two patients developed cholecystitis in the setting of cholelithiasis: 1 before CSEMS removal and 1 at 10 months after CSEMS removal, and both underwent cholecystectomy.
CSEMSs were left in place for a median time of 4 months (range 1-28 months) in 65 patients and were removed once successful treatment was confirmed by symptom resolution, LFT normalization (Figs. 3 to 5) (P Z .001), and repeat imaging. Patients were followed after CSEMS removal for a median of 12 months (range 3-26 months). Three patients developed a stricture in the uncovered proximal portion, 3 failed primary therapy, and 2 developed duodenal edema that prevented CSEMS removal, resulting in a success rate of 59 of 65 (90%). When a breakdown by
etiology of stricture was performed (Fig. 6), 17 of 22 patients (77%) with chronic pancreatitis, 15 of 16 patient (94%) with anastomotic stricture after liver transplant, and 27 of 27 patients (100%) with BBS from other etiology responded to treatment at the end of the study. An intent-to-treat global success rate of 59 of 79 (75%) was computed if patients who were lost to follow-up, developed duodenal edema that prevented CSEMS removal, developed cancer, or expired were considered failures. Logistical regression analysis failed to identify any factor predictive of success (eg, patient age, time in place, CSEMS length, and etiology). Of the 14 patients who did not undergo CSEMS removal during the study period, 3 were lost to followup, 1 developed hepatocellular carcinoma; 3 developed pancreatic cancer; 2 developed duodenal inflammation, which prevented access to the second portion for CSEMS removal; and 5 died from unrelated causes (1 urinary sepsis, 1 decompensated alcoholic cirrhosis, and 3 sudden deaths related to coronary heart disease). The 2 patients with duodenal edema received enteral feeding through a PEG jejunostomy until the inflammation completely resolved. The 6 patients who failed CSEMS treatment received plastic stents (4) or repeat CSEMS placement (2).
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Reinterventions and final results
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Figure 4. ALK level before CSEMS placement and after CSEMS removal.
Figure 2. Placement of a CSEMS (10 80 mm) across the stricture with excellent biliary decompression (patient A).
Figure 5. ALT level before CSEMS placement and after CSEMS removal.
Plastic stents have frequently been used in the management of patients with BBS.9-12,24 Plastic stents appear to
provide a long term resolution in a minority of patients with strictures caused by chronic pancreatitis,6,25 whereas patients with postoperative injury require repeat interventions over a long time period7 or an approach that maximizes the number of large-diameter plastic stents placed.11 Indeed, plastic stents have limited patency rates, becoming occluded within 3 to 6 months, requiring frequent replacement and increasing numbers of stents.11 The major factor that limits plastic-stent patency is the formation of a bacterial biofilm that leads to deconjugation of bile-acid salts, with sludge and stone formation related to the stent.26-28 Efforts to prolong plastic-stent patency by changing stent design29,30 by administering ursodeoxycholic acid, aspirin, or antibiotics27,29,31,32 have had little impact on patency rates in vivo. Recent studies confirmed the implication of duodenobiliary reflux,33 with dietary fiber forming a filter within the stent.34 This may explain why large-diameter stents have improved
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Figure 3. Total bilirubin (TB) level before CSEMS placement and after CSEMS removal.
DISCUSSION
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Figure 6. Long-term follow-up of the 79 patients who received CSEMSs with final long-term resolution provided. (CP, chronic pancreatitis; BC, biliary calculi; OLT, orthotopic liver transplant; INFL, inflammatory; SURG, surgical; Neo, neoplasia; LTF, lost to follow-up, DUOD INFL, duodenal inflammation).
TABLE 2. Series reporting CSEMS placement for BBS
Study
No. patients/ no. stents Etiology
Stent type
Time to removal, median (range) 5.25 mo (3-6 mo)
Bruno et al,46 2005
4/4
CP
Fully covered
Tringali et al,53 2005
6/6
CP
PCM
N/A
Cantu, et al,48 2005
14/14
CP
PCM
3/4
OTL
Fully covered
Kuo et al,47 2006
Reason for removal (no. of stents)
Resolution
Complications (no. of patients)
Per operator (4)
75% at removal
Prox migration (1)
N/A
2 CSEMS patent at 35-mo fup
Not reported
21 mo (18-33 mo)
Hyperplasia (5), migration (2), not removed (7)
37.5% at 30-mo fup
Cholestasis (7), cholangitis (5), duod migration (2), cholecystitis (1)
32 d (0-49 d)
Misplacement (1); per operator (2)
100% at removal
Septicemia (1), misplacement (1)
CP, Chronic pancreatitis; Prox, proximal; PCM, partially covered metal; N/A, not available; fup, follow-up; duod, duodenal; OTL, orthotopic liver transplantation.
patency rates compared with smaller-diameter stents. The diameter of plastic stents is limited by the accessory channel dimension, and this, in part, led to the development of SEMSs. For more than a decade, SEMSs have been the accepted therapy for palliation of malignant biliary obstruction,13-16,35 but their role in benign biliary disease remains controversial. Uncovered SEMS placement for BBS has been reported,7,36,37 but its acceptance has been limited by the observation of benign hyperplasia that
compromised patency.38 Despite their limitations, there is some support for the use of uncovered SEMSs in the management of refractory benign strictures.39 Not surprisingly, studies that compared surgery with uncovered SEMSs demonstrated that surgery is superior, primarily because of issues of patency and poor removability with uncovered SEMSs.40 Some investigators argue that the use of uncovered SEMSs in BBS should be avoided in patients with a life expectancy longer than 2 years.41
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Stents in benign biliary strictures
Figure 7. Distal biliary stricture related to chronic pancreatitis (patient C).
In an attempt to improve the durability of patency, coverings were proposed for SEMSs,42,43 with good effect. Their improved patency, compared with uncovered SEMSs,19 combined with the theoretical ability to remove CSEMSs, led to studies that assessed their utility in the setting of benign distal biliary strictures23,44 (Table 2). Trentino et al45 described placement of a CSEMS and its removal 6 months later in a patient with an anastomotic stricture after orthotopic liver transplantation. A study that evaluated 4 patients with chronic pancreatitis–associated biliary strictures found that removal of a fully covered CSEMS (Hanaro endoprosthesis; M.I. Tech Corporation, Seoul, South Korea) was feasible up to 6 months after placement and found resolution of biliary strictures in 3 of 4 patients after removal.46 In a recent series by Kuo et al,47 the investigators describe percutaneous placement of a CSEMS (Viabil; W.L. Gore and Associates, Flagstaff, Ariz) in 3 patients with strictures after orthotopic liver transplantation, and 1 stricture of unknown etiology. One patient developed a biliary-hepatic arterial fistula in the contralateral side to the stent placement, which was treated successfully with coil embolization; and 1 patient developed infection, which was treated conservatively. All CSEMSs were removed percutaneously except 1 removed by combined antegrade and retrograde approach. Interestingly, in that study, there were no episodes of CSEMS migration, and all stents remained patent for the duration of placement. Cantu et al48 published a series that evaluated CSEMSs in BBS that resulted from chronic pancreatitis; 14 patients underwent partially covered Wallstent (Boston Scientific, Natick, Mass) placement with no intention to remove. All stents remained patent 18 months after placement, but, in the ensuing period of observation, with a median follow-up of 22 months, half developed stent dysfunction
secondary to tissue hyperplasia (5 patients) and stent migration (2 patients). One patient developed cholecystitis, despite CSEMS deployment below the cystic-duct insertion. By design, all CSEMSs were left in place until the patients developed symptoms of stent dysfunction. Only 1 migrated CSEMS was removed; resolution of the biliary stricture was observed. In our study, CSEMSs were left in place until the study criteria for success were met. Sixty-five patients had CSEMSs removed after a median of 4 months; 59 of these had stricture resolution, without the need for further biliary intervention (Figs. 7 to 9). This provides a success rate of 59 of 65 (90%), because 2 patients developed duodenal edema, which prevented CSEMS removal. If the patients who were lost to follow-up, developed duodenal edema, cancer, or expired were considered failures, then an intent-to-treat global success rate of 59 of 79 patients (75%) was obtained. This compares
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Figure 8. Placement of a CSEMS (10 60 mm) across the stricture in regard of the pancreatic stent placed (patient C).
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Figure 10. Normalization of the common hepatic duct enlargement 3 months later (patient B).
Figure 9. Enlargement of the common hepatic duct after CSEMS removal in a patient treated for an anastomotic stricture after liver transplant (patient B).
favorably with the long-term success rate reported in patients with chronic pancreatitis or after surgical strictures, estimated at 35%49,50 and 80%,51,52 respectively. Based on our experience, removal of Wallstents beyond 6 months is feasible but more challenging, potentially requiring grasping the interior of the CSEMS with a rat-tooth forceps. Another interesting observation is related to the temporary enlargement of the distal bile duct after CSEMS removal. This seems to resolve over time (Figs. 9 and 10). Early complications occurred in 8% (6 patients), half of them related to the stent. Late complication occurred in 14% (11 patients), 73% of them (8 patients) related to the stent. Eleven patients had distal CSEMS migration, 7 of whom had short (40 mm) CSEMSs; although the use of 60- and 80-mm stents appeared to decrease the risk, this observation was not statistically supported (P Z .252). CSEMS placement is associated with pancreatitis.18,19 In our study, 2 cases of pancreatitis were mild, which required only observation. One patient who presented 452 GASTROINTESTINAL ENDOSCOPY Volume 67, No. 3 : 2008
with pancreatitis complicated by pancreatic-duct disruption underwent CSEMS placement and subsequently developed an infected pseudocyst. The collection resolved with endoscopic decompression. This was the only patient in whom biliary sphincterotomy did not prevent postERCP pancreatitis. In most cases of chronic pancreatitis, stents were placed, in the same session, in ductal strictures that involved both pancreatic and biliary ducts, with the distal end of the pancreatic stent protruding beyond the CSEMS (Figs. 7 and 8). In conclusion, CSEMSs successfully treated the majority of patients with BBS, with infrequent recurrence after removal and with complication rates within an acceptable range. We do not recommend leaving Wallstents in place beyond 6 months. With the arrival of additional CSEMSs, cost can be anticipated to decrease, making this an even more attractive option for benign diseases. It remains to be demonstrated that CSEMS removability can be improved, migration decreased, and final success improved.
ACKNOWLEDGMENTS We thank Penny Bashlor, RN, and Kristi Ellen, RN, for their critical contribution in the clinical follow-up of the patients enrolled in this study. www.giejournal.org
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1. Lillemoe KD, Melton GB, Cameron JL, et al. Postoperative bile duct strictures: management and outcome in the 1990s. Ann Surg 2000;232:430-41. 2. Warshaw AL, Schapiro RH, Ferrucci JT Jr, et al. Persistent obstructive jaundice, cholangitis, and biliary cirrhosis due to common bile duct stenosis in chronic pancreatitis. Gastroenterology 1976;70:562-7. 3. Pitt HA, Kaufman SL, Coleman J, et al. Benign postoperative biliary strictures. Operate or dilate? Ann Surg 1989;210:417-25; discussion 426-7. 4. Nealon WH, Urrutia F. Long-term follow-up after bilioenteric anastomosis for benign bile duct stricture. Ann Surg 1996;223:639-45; discussion 645-8. 5. Davids PH, Tanka AK, Rauws EA, et al. Benign biliary strictures. Surgery or endoscopy? Ann Surg 1993;217:237-43. 6. Smits ME, Rauws EA, van Gulik TM, et al. Long-term results of endoscopic stenting and surgical drainage for biliary stricture due to chronic pancreatitis. Br J Surg 1996;83:764-8. 7. Dumonceau JM, Deviere J, Delhaye M, et al. Plastic and metal stents for postoperative benign bile duct strictures: the best and the worst. Gastrointest Endosc 1998;47:8-17. 8. Frattaroli FM, Reggio D, Guadalaxara A, et al. Benign biliary strictures: a review of 21 years of experience. J Am Coll Surg 1996;183:506-13. 9. Berkelhammer C, Kortan P, Haber GB. Endoscopic biliary prostheses as treatment for benign postoperative bile duct strictures. Gastrointest Endosc 1989;35:95-101. 10. Draganov P, Hoffman B, Marsh W, et al. Long-term outcome in patients with benign biliary strictures treated endoscopically with multiple stents. Gastrointest Endosc 2002;55:680-6. 11. Costamagna G, Pandolfi M, Mutignani M, et al. Long-term results of endoscopic management of postoperative bile duct strictures with increasing numbers of stents. Gastrointest Endosc 2001;54:162-8. 12. Davids PH, Rauws EA, Coene PP, et al. Endoscopic stenting for postoperative biliary strictures. Gastrointest Endosc 1992;38:12-8. 13. Davids PH, Groen AK, Rauws EA, et al. Randomised trial of self-expanding metal stents versus polyethylene stents for distal malignant biliary obstruction. Lancet 1992;340:1488-92. 14. Kaassis M, Boyer J, Dumas R, et al. Plastic or metal stents for malignant stricture of the common bile duct? Results of a randomized prospective study. Gastrointest Endosc 2003;57:178-82. 15. Knyrim K, Wagner HJ, Pausch J, et al. A prospective, randomized, controlled trial of metal stents for malignant obstruction of the common bile duct. Endoscopy 1993;25:207-12. 16. Wagner HJ, Knyrim K, Vakil N, et al. Plastic endoprostheses versus metal stents in the palliative treatment of malignant hilar biliary obstruction. A prospective and randomized trial. Endoscopy 1993;25: 213-8. 17. Katsinelos P, Paikos D, Kountouras J, et al. Tannenbaum and metal stents in the palliative treatment of malignant distal bile duct obstruction: a comparative study of patency and cost effectiveness. Surg Endosc 2006;20:1587-93.
18. Bezzi M, Zolovkins A, Cantisani V, et al. New ePTFE/FEP-covered stent in the palliative treatment of malignant biliary obstruction. J Vasc Interv Radiol 2002;13:581-9. 19. Isayama H, Komatsu Y, Tsujino T, et al. A prospective randomised study of ‘‘covered’’ versus ‘‘uncovered’’ diamond stents for the management of distal malignant biliary obstruction. Gut 2004;53:729-34. 20. Wamsteker EJ, Elta GH. Migration of covered biliary self-expanding metallic stents in two patients with malignant biliary obstruction. Gastrointest Endosc 2003;58:792-3. 21. Matsushita M, Takakuwa H, Nishio A, et al. Open-biopsy-forceps technique for endoscopic removal of distally migrated and impacted biliary metallic stents. Gastrointest Endosc 2003;58:924-7. 22. Minami A, Fujita R. A new technique for removal of bile duct stones with an expandable metallic stent. Gastrointest Endosc 2003;57:945-8. 23. Kahaleh M, Tokar J, Le T, et al. Removal of self-expandable metallic Wallstents. Gastrointest Endosc 2004;60:640-4. 24. Huibregtse K, Katon RM, Tytgat GN. Endoscopic treatment of postoperative biliary strictures. Endoscopy 1986;18:133-7. 25. Barthet M, Bernard JP, Duval JL, et al. Biliary stenting in benign biliary stenosis complicating chronic calcifying pancreatitis. Endoscopy 1994;26:569-72. 26. Coene PP, Groen AK, Cheng J, et al. Clogging of biliary endoprostheses: a new perspective. Gut 1990;31:913-7. 27. Sung JY, Shaffer EA, Costerton JW. Antibacterial activity of bile salts against common biliary pathogens. Effects of hydrophobicity of the molecule and in the presence of phospholipids. Dig Dis Sci 1993;38:2104-12. 28. Leung JW, Ling TK, Kung JL, et al. The role of bacteria in the blockage of biliary stents. Gastrointest Endosc 1988;34:19-22. 29. England RE, Martin DF, Morris J, et al. A prospective randomised multicentre trial comparing 10 Fr Teflon Tannenbaum stents with 10 Fr polyethylene Cotton-Leung stents in patients with malignant common duct strictures. Gut 2000;46:395-400. 30. Costamagna G, Mutignani M, Rotondano G, et al. Hydrophilic hydromer-coated polyurethane stents versus uncoated stents in malignant biliary obstruction: a randomized trial. Gastrointest Endosc 2000;51: 8-11. 31. Libby ED, Leung JW. Ultrasmooth plastic to prevent stent clogging. Gastrointest Endosc 1994;40:386-7. 32. Ghosh S, Palmer KR. Prevention of biliary stent occlusion using cyclical antibiotics and ursodeoxycholic acid. Gut 1994;35:1757-9. 33. Weickert U, Venzke T, Konig J, et al. Why do bilioduodenal plastic stents become occluded? A clinical and pathological investigation on 100 consecutive patients. Endoscopy 2001;33:786-90. 34. van Berkel AM, van Marle J, Groen AK, et al. Mechanisms of biliary stent clogging: confocal laser scanning and scanning electron microscopy. Endoscopy 2005;37:729-34. 35. Prat F, Chapat O, Ducot B, et al. A randomized trial of endoscopic drainage methods for inoperable malignant strictures of the common bile duct. Gastrointest Endosc 1998;47:1-7. 36. Yamaguchi T, Ishihara T, Seza K, et al. Long-term outcome of endoscopic metallic stenting for benign biliary stenosis associated with chronic pancreatitis. World J Gastroenterol 2006;12:426-30. 37. Irving JD, Adam A, Dick R, et al. Gianturco expandable metallic biliary stents: results of a European clinical trial. Radiology 1989;172:321-6. 38. Wadhwa RP, Kozarek RA, France RE, et al. Use of self-expandable metallic stents in benign GI diseases. Gastrointest Endosc 2003;58:207-12. 39. Jeng KS, Sheen IS, Yang FS. Are expandable metallic stents better than conventional methods for treating difficult intrahepatic biliary strictures with recurrent hepatolithiasis? Arch Surg 1999;134:267-73. 40. Lopez RR Jr, Cosenza CA, Lois J, et al. Long-term results of metallic stents for benign biliary strictures. Arch Surg 2001;136:664-9. 41. Siriwardana HP, Siriwardena AK. Systematic appraisal of the role of metallic endobiliary stents in the treatment of benign bile duct stricture. Ann Surg 2005;242:10-9. 42. Shim CS, Lee YH, Cho YD, et al. Preliminary results of a new covered biliary metal stent for malignant biliary obstruction. Endoscopy 1998; 30:345-50.
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DISCLOSURES The following authors report that they have no disclosures relevant to this publication: B. Behm, B. W. Clarke, A. Brock, V. M. Shami, S. A. De La Rue, V. Sundaram, J. Tokar, R. B. Adams. The following authors have disclosed actual or potential conflicts: M. Kahaleh has received grant support from Boston Scientific, Alveolus, and Cook Medical. P. Yeaton has received grant support from Olympus and Alveolus.
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Received November 9, 2006. Accepted June 25, 2007. Current affiliations: Digestive Health Center (M.K., B.B., B.W.C., A.B., V.M.S., S.D.L.R., V.S., J.T., P.Y.), the Department of Surgery (R.B.A.), University of Virginia Health System, Charlottesville, Virginia, USA. Presented at Digestive Disease Week, Chicago, Illinois, May 14-18, 2005, and Washington, DC, May 20-23, 2007 (Gastrointest Endosc 2005;61: AB208, Gastrointest Endosc 2007;65:AB123). Reprint requests: Michel Kahaleh, MD, Digestive Health Center Box 800708, University of Virginia Health System, Charlottesville, VA 22908-0708.