The Treatment of Patients with Symptomatic Common Bile Duct Stenosis Secondary to Chronic Pancreatitis Using Partially Covered Metal Stents: A Pilot Study

• Introduction
• Patients and Methods
• Patients
• Endoscopic Treatment
• Follow-Up
• Statistical Analysis
• Results
• Endoscopic Treatment
• Early Follow-Up
• Late Follow-Up
• Discussion
• Acknowledgments
• References

Background and Study Aims: Although surgery remains the gold standard for the treatment of symptomatic common bile duct stenosis associated with chronic pancreatitis, plastic and self-expandable open-mesh stents have been proposed as alternative treatments. These may dysfunction, however, mainly due to stent occlusion by clogging or by hyperplasia of inflammatory tissue. The aim of this study was to evaluate the safety and long-term results of using partially covered metal stents in this setting.
Patients and Methods: A total of 14 patients (12 men, 2 women; mean age 50 ± 3 years) underwent partially covered metal stent insertion for common bile duct stenosis secondary to chronic pancreatitis (12 alcohol-related, two idiopathic). They had all been treated previously with plastic prostheses.
Results: Either a 40-mm (n = 13) or a 60-mm (n = 1) partially covered metal stent was placed, depending on the length of the common bile duct stenosis and the level of the cystic duct bifurcation. Stent placement was successful, with resolution of cholangitis and improvement in cholestasis, in all patients. During the median follow-up period of 22 months (range 12 - 33 months) seven patients developed dysfunction of the stent and required re-treatment. At 12, 24, and 30 months, the stent patency rates were 100 %, 40 %, and 37.5 % respectively.
Conclusions: While partially covered metal stenting is safe and effective for the initial treatment of chronic pancreatitis-associated common bile duct stenosis and shows promising short-term results, long-term data show that dysfunction occurs in 50 % of cases. In light of the continued interest in nonsurgical treatment of this condition, further research is warranted to investigate new stent designs with improved long-term patency.

Introduction

Benign strictures of the common bile duct (CBD) have been reported in up to 30 % of patients with chronic pancreatitis [1] [2]. Stenosis develops in the distal (intrapancreatic) portion of the CBD [2] [3] [4] and occurs as a result of compression by periductal pancreatic tissue. Cholangitis, persistent cholestasis, and biliary cirrhosis may develop in these patients [3] [5] [6] and drainage of the biliary tree should be considered when there is cholestasis (found in 8 % of patients). Hammel et al. [7] reported regression of hepatic fibrosis after surgical biliary drainage in patients with CBD stenoses secondary to chronic pancreatitis, providing further evidence in support of performing biliary drainage in this group of patients. Traditionally, treatment by biliary diversion surgery has been considered to be the gold standard in this condition but this is associated with significant perioperative mortality and morbidity [8] [9], mainly due to sepsis and associated co-morbidity. Endoscopic treatment is indicated for patients who are unfit for surgery but may also have potential as initial therapy in patients who are undergoing endotherapy of the pancreas [5]. Plastic stents have been used in this situation but their use is limited by occlusion, which tends to occur after 3-6 months, and spontaneous migration [5], and frequent hospitalization may be required for stent replacement. Recent studies have suggested increased efficacy using multiple plastic stents, presumably as a result of the larger cumulative diameter [10] [11] [12].

Self-expandable metal stents (SEMS) have a larger inner diameter after complete expansion than plastic stents (30 Fr vs. ≤ 11.5 Fr). This is thought to account for the longer-lasting patency associated with SEMS which was demonstrated in two randomised trials involving patients with CBD stenoses secondary to malignancies [13] [14]. However, dysfunction occurs secondary to tumour ingrowth through the ”open” meshes in these stents and re-treatment is required in 22 % - 28 % of cases [13] [14]. SEMS are clearly not indicated in postoperative benign strictures as ”calibration” is achieved in most patients using multiple plastic stents [11]. In chronic pancreatitis-associated CBD stenosis, however, the effectiveness of plastic stents in achieving long-term calibration is poor. The potential of SEMS in high-risk patients is therefore still debatable. Even though SEMS are not removable prostheses, they have recently been studied in the treatment of benign CBD stenosis [15] [16] [17] [18], but occlusion due to inflammatory hyperplasia remains a major problem. In an attempt to prevent ingrowth, SEMS with a nonporous covering membrane have been developed [19] and tested in patients with malignant obstructions of the CBD [20] [21] [22]. A partially covered metal (PCM) stent with uncovered metal meshes at both ends (0.5 cm long) was then designed to provide better anchorage [23], with the aim of reducing migration while still preventing most of the tissue ingrowth.

The aim of the present study was to evaluate the safety, effectiveness, and long-term results of PCM stenting in CBD stenoses secondary to chronic pancreatitis.

Patients and Methods

Patients

Between February 2001 and June 2003, 14 patients (12 men, 2 women; mean age 50, range 36 - 65) were evaluated with a view to PCM stent placement for symptomatic CBD stenosis secondary to severe chronic pancreatitis. The patients’ charts were reviewed and their age at diagnosis of chronic pancreatitis, the etiology of the chronic pancreatitis, and the timing and type of previous endoscopic treatments were recorded (Table [1]). The median duration of the disease was 60±24 months (range 12-228 months). No patients had undergone biliary surgery (excluding cholecystectomy) or pancreatic surgery in the past. All the patients had undergone previous endoscopic treatments (biliary sphincterotomy and plastic stent placement) for symptomatic CBD stenosis. Prior to PCM stent placement, these patients had undergone a median of 3.1 replacements (ranging from one to seven) of 10-Fr plastic stents at intervals of 4.0 ± 1.4 months for clogging, migration, or scheduled stent exchange. The mean pre-PCM stent placement alkaline phosphatase level was 1010 ± 314 U/L and the mean pre-PCM stent placement total bilirubin level was 2.1 ± 0.6 mg/dl and nine patients presented with overt cholangitis. Three patients were unfit for surgery (due to portal thrombosis and cavernoma in two patients and recent myocardial infarction in one patient).

Each patient was discussed at a multidisciplinary meeting and formal consent for endoscopic treatment, including PCM stenting of the CBD, was obtained from all patients.

Endoscopic Treatment

After removal of nonfunctional plastic stents, cholangiography was performed to analyze the morphology and length of the CBD stenosis, classified according to Caroli & Nora [4], and the level of the cystic duct bifurcation. A partially covered metal stent (Wallstent, Boston Scientific, Natick, Massachussetts, USA) was deployed as described for SEMS in a previous study [24]: in brief, a stent-carrying catheter was passed over a guide wire which had been inserted previously into the intrahepatic biliary ducts; the outer layer of the system was progressively withdrawn in order to allow expansion of the stent, with the distal end level with the papillary orifice. Stent placement was considered to have been technically successful when: a) the PCM stent was positioned across the entire stenosis; b) only the distal uncovered portion was in a transpapillary position; c) increased bile flow was observed after deployment; and d) complete outflow of the contrast medium from the biliary tree (excluding the gallbladder) was visualized during cholangiography at the end of the procedure (Figure [1]).

Follow-Up

Patients were hospitalized for at least 24 hours and then discharged if they were pain-free. Biochemical blood analyses were repeated within 7 days after treatment (early follow-up) and subsequently at clinical evaluation check-ups at 3-month intervals or when symptoms reappeared (late follow-up). At follow-up evaluations, patients underwent abdominal computed tomography or secretin-enhanced magnetic resonance cholangiopancreatography in order to assess PCM stent function and to detect other possible complications of chronic pancreatitis. Dysfunction of the PCM stent was defined as the presence of symptoms (of jaundice or cholangitis) and/or persistent significant cholestasis with radiological evidence of dilatation of the biliary tree.

Statistical Analysis

The results are presented as means and standard error of the mean or as median and interquartile range, according to data distribution. Patients were censored at the time of stent dysfunction or, in the absence of dysfunction, at last follow-up. Stent patency was calculated by dividing the number of patients with patent stents at each predetermined point during follow-up by the sum of the patients who had experienced stent dysfunction plus the patients with patent stents at that time.

Results

Endoscopic Treatment

Type I and type III stenoses (defined according to Caroli & Nora’s classification [4]), were visualized in nine and five patients respectively. A 40-mm PCM stent was inserted in 13 patients and a 60-mm PCM stent was inserted in one patient, selected according to the stricture length and the level of the cystic bifurcation in order to avoid obstruction of the cystic duct by the covered portion of the stent. Insertion of the stent was considered to be optimal in 13/14 patients (93 %); in one patient, the position of the stent after the procedure was judged to be suboptimal, with the distal portion migrating 1 cm out of the papilla, but there was no dysfunction.

Early Follow-Up

In all patients, cholangitis resolved and cholestasis improved soon after endoscopic treatment. In one patient with pre-existing hydropic gallbladder containing sludge, cholecystitis developed even though the covered portion of the stent did not occlude the cystic duct at the bifurcation: 4 days after placement of the stent, he underwent cholecystectomy without any problems. The other 13 patients were discharged after a median hospital stay of 1 day (range 1-7 days).

Late Follow-Up

Patients were followed up for a median period of 22 months (range 12-33 months). Stent dysfunction developed in seven patients (50 %), at a median time of 21 months (range 18-33 months). All patients with stent dysfunction experienced recurrent cholestasis, and five patients presented with cholangitis. Subsequent therapeutic endoscopic retrograde cholangiopancreatography reported hyperplastic ingrowth (n = 5) or migration (n = 2) of the PCM stent. In patients with hyperplasia, therapeutic options included: diathermy (n = 3; Figure [2]); the placement of plastic biliary stents within the PCM stent (n = 2); and surgical biliary diversion (n = 1), which was successful and unaffected by the presence of the PCM stent. Migration of the PCM stent occurred in two patients. The first patient presented with cholangitis 18 months after PCM stent placement, when endoscopy revealed that the stent had migrated distally and a significant portion was intraduodenal. The stent was removed without any problems using a polypectomy snare. Cholangiography showed resolution of the stenosis and no further biliary intervention was necessary. The second patient presented with cholangitis at 33 months. Endoscopic retrograde cholangiopancreatography revealed that the PCM stent had migrated 1 cm internally and that there was a distal biliary stricture. A second PCM stent was placed to bridge the distal stricture and the patient has not experienced any further problems.

There was no significant difference in the duration of follow-up between patients with and patients without PCM stent dysfunction (21 months, range 18 - 33 months vs. 23 months, range 12 - 32 months; Mann-Whitney U test, P = 0.48). Stent patency after PCM stent placement was 100 % after 12 months, 40 % at 24 months, and 37.5 % at 30 months (Figure [3]).

Discussion

This is the first reported series of patients with a symptomatic benign CBD stenosis secondary to severe chronic pancreatitis who were treated using a PCM stent. Although the results in the first 12-18 months were promising (with a 100 % patency rate), 50 % of the patients subsequently developed dysfunction. In this study we used a stent which remains patent for longer than the traditional plastic stents and one that does not preclude future surgical biliary diversion. We recommend biliary surgery when there are clinical indications for drainage and when diversional or resective pancreatic surgery for cure or palliation (main pancreatic duct drainage, symptomatic duodenal obstruction, suspected pancreatic neoplasia) has been planned, or when endoscopic therapy has failed.

To date, there have been no randomised trials comparing surgery and endoscopic treatment. In this clinical setting, surgery is associated with significant mortality and morbidity [8] [9], hospital stay, and social cost. In patients who are unfit for or who refuse surgery, biliary sphincterotomy and placement of a plastic stent is the therapy of choice. This treatment is also highly effective in the short term in younger patients who are fit for surgery [5], but they will require lifelong replacements of the stents due to clogging and spontaneous migration and there is a risk of cholangitis due to stent clogging. The results of biliary plastic stenting in severe chronic pancreatitis after removal are disappointing, with a rate of persistent clinical remission with radiological and biochemical recovery of only 10 % - 28 % [5] [25] [26] [27] [28]. Pozsar et al. [12] treated 29 patients with CBD strictures secondary to chronic pancreatitis with an increasing number of plastic stents. They reported unresolved stenosis in 30 % of cases and biochemical and radiological remission in 60 % (of stent-free patients), after a mean of 12.1 months from when the stents were removed. Catalano et al. [10] recently reported improved resolution of CBD strictures secondary to chronic pancreatitis using multiple plastic stents in 12 patients, with a mean follow-up period of 3.9 years. Although encouraging, these results should be confirmed by larger studies with a longer duration of follow-up.

Covered metal stents are currently used in the palliative treatment of distal CBD stenosis secondary to malignancies [20] [21] [22]. The covering membrane is designed to prevent ingrowth of neoplastic tissue, but at the same time it prevents mucosal imbedding into the meshes and so these stents are associated with an increased risk of spontaneous migration [21] [22] [29]. At present, our knowledge about the overall patency rates of covered stents is limited by the short survival of patients with unresectable malignancies. Born et al. [23] reported a patency rate of 60 %, but in that series of ten patients, death occurred at a mean of 6 months after stent placement and in seven of these patients there was no apparent dysfunction of the PCM stent, thus resulting in a possible underestimation of the median patency rate. At the same point of follow-up in our series, the patency rate was 100 % and dysfunction did not occur until 18 months after stent insertion. However, given the differences in the etiology of the biliary strictures in the two studies, such comparisons must be made cautiously.

In our series, stent dysfunction occurred late (after 18 months) and resulted from hyperplasia and migration. Dysfunction was treated endoscopically in six of the patients. One patient had the PCM stent removed because of distal migration, as described previously [29]. Interestingly, the stricture had resolved and no further biliary intervention was necessary. We prefer to remove distally migrated stents in order to avoid damage to the duodenal wall (ulceration, perforation) [30] [31]. One patient was treated by surgical biliary diversion and the presence of the short, distal metallic stent did not present any difficulties during the hepaticojejunostomy.

In conclusion, while PCM stents for CBD strictures secondary to chronic pancreatitis are safe and effective in the short term, stent dysfunction occurs in a significant proportion of patients during late follow-up. Although the duration of patency is certainly longer than that seen with plastic biliary stents, it is still somewhat disappointing in light of the chronic nature of the disease and the need for further interventions. Further work needs to be done in the development of a SEMS that effectively prevents hyperplasia and can be used in such long-term situations.

Acknowledgments

Dr P. Cantù was supported by a grant from the Chair of Gastroenterology, University of Milan, IRCCS Ospedale Maggiore, Milan, Italy, and Dr L. C. Hookey is supported by the Canadian Association of Gastroenterology/CIHR/Solvay Pharma Inc. Fellowship Award.

References

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• 28 Smits M E, Rauws E AJ, Van Gulik T M. et al . Long-term results of endoscopic stenting and surgical drainage for biliary stricture due to chronic pancreatitis.  Br J Surg. 1996;  83 764-768
  Search in Google Scholar
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J. Devière, M. D.

Department of Gastroenterology

Erasme University Hospital · Rue de Lennik 808 · 1070 Brussels · Belgium

Fax: +32-02-555-4697

Email: jdeviere@ulb.ac.be

References

• 1 Afroudakis A, Kaplowitz N. Liver histopathology in chronic common bile duct stenosis due to chronic alcoholic pancreatitis.  Hepatology. 1981;  1 65-72
  CrossrefPubMedSearch in Google Scholar
• 2 Scott J, Summerfield J A, Elias E. et al . Chronic pancreatitis: a cause of cholestasis.  Gut. 1977;  18 196-201
  PubMedSearch in Google Scholar
• 3 Littenberg G, Afroudakis A, Kaplowitz N. Common bile duct stenosis from chronic pancreatitis: a clinical and pathologic spectrum.  Medicine. 1979;  58 385-412
  PubMedSearch in Google Scholar
• 4 Sarles H, Sahel J. Cholestasis and lesions of the biliary tract in chronic pancreatitis.  Gut. 1978;  19 851-857
  CrossrefPubMedSearch in Google Scholar
• 5 Devière J, Devaere S, Baize M, Cremer M. Endoscopic biliary drainage in chronic pancreatitis.  Gastrointest Endosc. 1990;  36 96-100
  CrossrefPubMedSearch in Google Scholar
• 6 Stahl T J, Allen M O, Ansel H J, Vennes J A. Partial biliary obstruction caused by chronic pancreatitis.  Ann Surg. 1988;  207 26-32
  PubMedSearch in Google Scholar
• 7 Hammel P, Couvelard A, O’Toole D. et al . Regression of liver fibrosis after biliary drainage in patients with chronic pancreatitis and stenosis of the common bile duct.  N Engl J Med. 2001;  344 418-423
  CrossrefPubMedSearch in Google Scholar
• 8 Aranha G V, Prinz R A, Freeark R J, Greenlee H B. The spectrum of biliary tract obstruction from chronic pancreatitis.  Arch Surg. 1984;  119 595-600
  PubMedSearch in Google Scholar
• 9 Stabile B E, Calabria R, Wilson S E, Passaro E. Stricture of the common bile duct from chronic pancreatitis.  Surg Gynecol Obstet. 1987;  165 121-126
  PubMedSearch in Google Scholar
• 10 Catalano M F, Linder J D, George S. et al . Treatment of symptomatic distal common bile duct stenosis secondary to chronic pancreatitis: comparison of single vs. multiple simultaneous stents.  Gastrointest Endosc. 2004;  60 945-952
  CrossrefPubMedSearch in Google Scholar
• 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;  54 162-168
  CrossrefPubMedSearch in Google Scholar
• 12 Pozsar J, Sahin P, Laszlo F. et al . Medium-term results of endoscopic treatment of common bile duct strictures in chronic calcifying pancreatitis with increasing numbers of stents.  J Clin Gastroenterol. 2004;  38 118-123
  CrossrefPubMedSearch in Google Scholar
• 13 Davids P H, Groen A K, Rauws E AJ. et al . Randomised trial of self-expanding metal stents versus polyethylene stents for distal malignant biliary obstruction.  Lancet. 1992;  340 1488-1492
  CrossrefPubMedSearch in Google Scholar
• 14 Knyrim K, Wagner H J, Pausch J, Vakil N. A prospective, randomised, controlled trial of metal stents for malignant obstruction of the common bile duct.  Endoscopy. 1993;  25 207-212
  Thieme ConnectPubMedSearch in Google Scholar
• 15 Devière J, Cremer M, Baize M. et al . Management of common bile duct stricture caused by chronic pancreatitis with metal mesh self-expandable stents.  Gut. 1994;  35 122-126
  CrossrefPubMedSearch in Google Scholar
• 16 Dumonceau J M, Nicase N, Devière J. The ultraflex Diamond stent for benign bliary obstruction.  Gastroint Endosc Clin N Am. 1999;  9 541-545
  PubMedSearch in Google Scholar
• 17 O’Brien S M, Hatfield A RW, Craig P I, Williams S P. A 5-year follow-up of self-expanding metal stents in the endoscopic management of patients with benign bile duct strictures.  Eur J Gastroenterol Hepatol. 1998;  10 141-145
  CrossrefPubMedSearch in Google Scholar
• 18 Van Berkel A M, Cahen D L, Van Westerloo D J. et al . Self-expanding metal stents in benign biliary strictures due to chronic pancreatitis.  Endoscopy. 2004;  36 381-384
  Thieme ConnectPubMedSearch in Google Scholar
• 19 François E, Devière J. Endoscopic retrograde cholangiopancreatography.  Endoscopy. 2002;  34 882-887
  Thieme ConnectPubMedSearch in Google Scholar
• 20 Isayama H, Komatsu Y, Tsujino T. et al . Polyurethane-covered metal stent for management of distal malignant biliary obstruction.  Gastrointest Endosc. 2002;  55 366-370
  CrossrefPubMedSearch in Google Scholar
• 21 Shim C S, Lee Y H, Cho Y D. et al . Preliminary results of a new covered biliary metal stent for malignant biliary obstruction.  Endoscopy. 1998;  30 345-350
  PubMedSearch in Google Scholar
• 22 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;  53 729-734
  CrossrefPubMedSearch in Google Scholar
• 23 Born P, Neuhaus H, Rosch T. et al . Initial experience with a new, partially covered Wallstent for malignant biliary obstruction.  Endoscopy. 1996;  28 699-720
  Thieme ConnectPubMedSearch in Google Scholar
• 24 Cremer M, Devière J, Sugai B, Baize M. Expandable biliary metal stents for malignancies: endoscopic insertion and diathermic cleaning for tumor ingrowth.  Gastrointest Endosc. 1990;  36 451-457
  PubMedSearch in Google Scholar
• 25 Barthet M, Bernard J P, Duval J L. et al . Biliary stenting in benign biliary stenosis complicating chronic calcifying pancreatitis.  Endoscopy. 1994;  26 569-572
  Thieme ConnectPubMedSearch in Google Scholar
• 26 Farnbacher M J, Rabenstein T, Ell C. et al . Is endoscopic drainage of common bile duct stenoses in chronic pancreatitis up-to-date?.  Am J Gastroenterol. 2000;  95 1466-1471
  CrossrefPubMedSearch in Google Scholar
• 27 Kahl S, Zimmermann S, Glasbrenner B. et al . Treatment of benign biliary strictures in chronic pancreatitis by self-expandable metal stents.  Dig Dis. 2002;  20 199-203
  CrossrefPubMedSearch in Google Scholar
• 28 Smits M E, Rauws E AJ, Van Gulik T M. et al . Long-term results of endoscopic stenting and surgical drainage for biliary stricture due to chronic pancreatitis.  Br J Surg. 1996;  83 764-768
  Search in Google Scholar
• 29 Wamsteker E J, Elta J H. Migration of covered biliary self-expanding metallic stents in two patients with malignant biliary obstruction.  Gastrointest Endosc. 2003;  58 792-793
  CrossrefPubMedSearch in Google Scholar
• 30 Ee H, Laurence B H. Hemorrhage due to erosion of a metal biliary stent through the duodenal wall.  Endoscopy. 1992;  24 431-432
  PubMedSearch in Google Scholar
• 31 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;  58 924-927
  CrossrefPubMedSearch in Google Scholar

J. Devière, M. D.

Department of Gastroenterology

Erasme University Hospital · Rue de Lennik 808 · 1070 Brussels · Belgium

Fax: +32-02-555-4697

Email: jdeviere@ulb.ac.be