management of complications associated with partially covered biliary metal stents
TRANSCRIPT
ORIGINAL ARTICLE
Management of Complications Associated with Partially CoveredBiliary Metal Stents
Henry Ho Æ Anshu Mahajan Æ Sonia Gosain Æ Animesh Jain Æ Andrew Brock ÆMichele E. Rehan Æ Kristi Ellen Æ Vanessa M. Shami Æ Michel Kahaleh
Received: 11 December 2008 / Accepted: 3 February 2009 / Published online: 7 March 2009
� Springer Science+Business Media, LLC 2009
Abstract Background Partially covered metal stents
(PCMS) have been increasingly used for both malignant and
benign biliary indications. This study reports their compli-
cations and subsequent management. Methods Over 5 years,
all patients receiving biliary PCMS were followed pro-
spectively until stent-related dysfunction or death. Data
were analyzed for the following variables: primary disease,
time until revision, and type and reason for revision. Results
PCMS were placed in 396 patients (247 with malignant
biliary strictures and 149 with benign biliary disease).
Complications were observed in 70 patients (18%), occur-
ring a mean time following placement of 159 days.
Duodenal migration occurred in 27 cases (6.8%), while
proximal migration occurred in 9 cases (2.3%). Cholecys-
titis was documented in 13 cases (3.3%). There were six
cases of stent occlusion due to debris or sludge (1.6%), four
cases of pancreatitis (1%), four cases of tumor overgrowth
(1%), three cases of benign stenosis in the uncovered portion
of the PCMS (0.8%), two cases of abdominal pain (0.5%),
one case of an infected biloma (0.3%), and one case of a liver
abscess (0.3%). Conclusions Major complications associ-
ated with PCMS placement include migration and
cholecystitis. Their management includes endoscopic revi-
sion, cholecystectomy, and gallbladder drainage. Further
improvements in the structure and composition of PCMS
may prevent these complications.
Keywords ERCP: Endoscopic retrograde
cholangiopancreatography � SEMS: Self-expanding metal
stent � PCMS: Partially covered self-expanding metal stent
Introduction
Endoscopic retrograde cholangiopancreatography (ERCP)
with placement of biliary stents has been used for more
than 2 decades [1, 2]. Because of their lower cost, wide
distribution, and ease of placement, plastic stents have been
conventionally used for benign biliary diseases and
malignant biliary obstruction with short-term survival [2].
Those patients with malignant distal biliary obstruction and
survival time beyond 6 months have been more frequently
treated with self-expandable metal stents (SEMS), given
their greater complication-free survival and cost-effec-
tiveness [3–6]. In an attempt to improve patency, however,
partially covered metal stents (PCMS) were developed to
resist tissue in-growth through the stent interstices [7, 8], a
well-demonstrated complication of uncovered metal stents
[9]. Indeed, the demonstration of PCMS removability [10,
11] has prompted expanded indications for their use to
include placement for distal pancreatico-biliary malig-
nancy regardless of resectability [12, 13].
With the increasing use of PCMS, though, several
complications have been reported, including migration [12,
14–16], benign strictures [7, 17] and cholecystitis [18, 19].
Given the limited prospective data regarding PCMS and
their wider use in malignant and benign biliary diseases,
we sought to evaluate the complications associated with
their use as well as their respective management.
Patients and Methods
Patients
A total of 423 patients underwent insertion of metal
stents in our institution over a 5-year period and were
H. Ho � A. Mahajan � S. Gosain � A. Jain � A. Brock �M. E. Rehan � K. Ellen � V. M. Shami � M. Kahaleh (&)
Digestive Health Center, University of Virginia Health System,
Charlottesville, Box 800708, VA 22908-0708, USA
e-mail: [email protected]
123
Dig Dis Sci (2010) 55:516–522
DOI 10.1007/s10620-009-0756-x
followed prospectively; 27 patients received uncovered
SEMS and 396 received PCMS. All patients in the
uncovered SEMS group had malignant hilar lesions. In
the PCMS group, 247 patients presented with malignant
disease and 149 patients with benign disease. After stent
insertion, patients were followed in clinic with liver
function tests (LFTs) until stent removal (in cases of
benign diseases receiving PCMS), stent dysfunction, or
death. The study was approved by our institutional
review board; all patients provided written consent for
their procedures.
Methods
In the uncovered SEMS group, uncovered Wallstents (40,
60, or 80 mm length) of 10-mm diameter (Boston Scien-
tific, Natick, MA) were placed. In the PCMS group,
Wallstents (40, 60, or 80 mm length) of 10-mm diameter,
partially covered with Permalume� (Boston Scientific,
Natick, MA), were placed. Following biliary sphincterot-
omy, the origin of the cystic duct insertion was noted in
patients having a gallbladder. The PCMS delivery system
was advanced proximal to the lesion over a guidewire
where the PCMS was positioned and deployed. When
anatomically feasible, PCMS were deployed to avoid
occlusion of the cystic duct insertion when the gallbladder
was present. Removal of PCMS was effected using the
snare or rat tooth technique as previously published [10].
Proximal migration was managed with a combination of
CRE balloon dilation (Boston Scientific) and rat tooth
extraction (Figs. 1, 2, 3, 4, and 5).
Definition of Events
Successful PCMS placement was defined as deployment of
the PCMS across the lesion effecting biliary decompression
and relief of symptoms. Stent patency was defined by the
period of time between stent insertion and stent dysfunc-
tion. Stent occlusion, in contrast to tumor overgrowth or
stricture in the uncovered portions of the PCMS (hyper-
plasia), was defined as stent dysfunction secondary to
biliary debris or sludge. Complications were stratified as
early (occurring B30 days of PCMS placement) or late
(occurring [30 days following PCMS placement). Cho-
langitis was defined as fever persisting for 24 h in the
setting of biochemical cholestasis without another dis-
cernible cause. Cholecystitis was defined by appropriate
symptoms in the setting of supportive imaging (ultrasound,
computed tomography). We also distinguish duodenal from
proximal migration, hereto uncommonly cited in the
literature.
Repeat biliary intervention was defined as the need for any
type of endoscopic, percutaneous, or surgical procedure to
improve biliary drainage after insertion of the initial PCMS.
Fig. 1 Fluoroscopy showing CRE balloon dilation of a proximally
migrated PCMS
Fig. 2 Fluoroscopy showing the PCMS grasped from the inside using
a rat tooth forceps
Dig Dis Sci (2010) 55:516–522 517
123
Results
A total of 70 patients (41 males, 29 females) with a mean
age of 59 developed complications (18%) in the PCMS
group. Complications were observed in 48 patients with
underlying malignancy and 22 patients with benign biliary
diseases (Table 1). The global mean time to complication
was 159 days with a range between 1 and 1,027 days.
Early Complications (B30 Days) of PCMS and
Management
Fourteen patients (3.5%) had early complications. Five
patients had benign disease, and nine patients had malig-
nant indications (Table 2). Complications included
duodenal migration (n = 3), proximal migration (n = 2),
cholecystitis (n = 4), pancreatitis (n = 2), stent occlusion
(n = 1), tumor overgrowth (n = 1), and abdominal pain
(n = 1).
All the patients who suffered from early cholecystitis
had underlying malignant disease. Two patients were noted
to have had the PCMS covering the cystic duct insertion,
one had tumor involvement of the cystic duct, and only one
had PCMS below the cystic duct. Three patients were
treated with percutaneous cholecystostomies, while one
patient had a gallbladder stent placed endoscopically.
Twelve patients underwent PCMS revision. Two
patients who experienced stent migration were managed by
Fig. 3 Fluoroscopy showing successful extraction of the PCMS from
the bile duct
Fig. 4 Fluoroscopy showing removal of the PCMS through the
working channel of the endoscope
Fig. 5 Cholangiogram post PCMS removal showing enlargement of
the bile duct post PCMS removal
518 Dig Dis Sci (2010) 55:516–522
123
removal and replacement with plastic stents, while the
other three underwent replacement with a PCMS. The
patient with early stent occlusion was found to have a large
amount of debris within the PCMS and was treated with
removal and replacement with new PCMS. The one patient
with early tumor overgrowth was also managed by
replacement with PCMS. The two patients with pancreatitis
and the one experiencing abdominal pain as a result of
PCMS placement had their PCMS removed.
Late Complications ([30 Days) of PCMS
and Management
Table 3 delineates the 56 patients with long-term compli-
cations, of which 19 had benign indications and 37 had
malignant ones. Migration was observed in 31 patients
(7.8%). Duodenal migration occurred in 24 cases (6.1%),
whereas proximal migration occurred in 7 cases (1.7%).
The management of migration included replacement with
PCMS (n = 14), replacement with plastic stents (n = 5),
removal (n = 7), stent within a stent (n = 3), or no inter-
vention (n = 2) secondary to spontaneous migration with
resolution.
The second most common long-term complication of
PCMS placement was cholecystitis (n = 9). In six
patients, the PCMS covered the cystic duct insertion.
There was cancer involvement of the cystic duct in one
patient, while two patients who had PCMS placed below
the cystic duct developed cholecystitis. Cholecystitis was
managed by cholecystectomy in six cases, percutaneous
drainage in two cases, and placement of a gallbladder
stent in one case.
Three patients developed late cholangitis. They had
duodenal cancer, ampullary adenoma, and benign stricture
and developed cholangitis at 873, 874, and 1,027 days,
respectively. All three patients had their PCMS removed,
while the patient with duodenal cancer underwent PCMS
replacement.
Tumor overgrowth (n = 3) was managed by replace-
ment with plastic stents in two cases and replacement with
PCMS in the other. We also report PCMS stricture in the
proximal uncovered portion of the stent in three patients
(Fig. 6), all of which were in benign disease; two were
managed with replacement with PCMS, while one patient
received plastic stents.
Pancreatitis occurring after PCMS placement was
managed with PCMS removal. One patient developed a
liver abscess 364 days after PCMS placement and was
treated with removal of PCMS and replacement with
plastic stents. Another patient developed an infected bilo-
ma, 106 days after PCMS placement, which was related to
a bile leak after cholecystectomy. This patient had removal
and replacement with PCMS. Lastly, one patient developed
abdominal pain 45 days after PCMS placement. This was
managed with PCMS removal only, since the benign bili-
ary stricture had resolved.
Table 2 Early complications of PCMS insertion
Reason for revision No. Mean time to revision (days)
Duodenal migration 3 3
Proximal migration 2 10
Cholecystitis 4 9
Tumor overgrowth 1 24
Stent occulusion 1 7
Pancreatitis 2 11
Abdominal pain 1 5
Table 3 Long-term complications of PCMS insertion
Reason for revision No. Mean time to revision
(days)
Duodenal migration 24 185
Proximal migration 7 113
Cholecystitis 9 97
Tumor overgrowth 3 215
Cholangitis 3 925
Stricture in uncovered portion 3 262
Stent occlusion 2 136
Pancreatitis 2 50
Abdominal pain 1 45
GB fossa abscess 1 106
Liver abscess 1 364
Table 1 Characteristics of patients at the time of PCMS insertion
Characteristics No.
No. of patients 70
Gender (male/female) 41/29
Mean age (years, range) 59 (23–89)
Primary disease
Pancreatic cancer 35
Benign stricture 20
Cholangiocarcinoma 4
Ampullary adenoma 3
Duodenal cancer 3
Bile leak 2
Pancreatic lymphoma 1
Gastric lymphoma 1
Ampullary carcinoma 1
Dig Dis Sci (2010) 55:516–522 519
123
Discussion
Expandable biliary metal stents have been developed for
the treatment of malignant biliary strictures [3–6]. In the
past decade, partially covered self expandable metal stents
(PCMS) were developed to prevent tumor growth through
the mesh of the stent [20]. Experience with PCMS has been
reported by several groups [11, 17, 21–25].
PCMSs provide better biliary decompression than plas-
tic stents because of their larger diameter. In addition,
PCMSs have a metal composite covered by a synthetic
material, such as silicone, that resists the effects of bile,
gastric, or pancreatic secretions [26]. The covering is
designed to prevent tumor ingrowth [7, 8], while the 0.5-
mm uncovered portions at each end of the stent are meant
to prevent migration. Our group has a preference for PCMS
for distal biliary lesions, leaving the use of uncovered
SEMS for malignant hilar lesions of the biliary tree deemed
surgically unresectable. This explains the small number of
uncovered SEMS placed during the study period.
In the PCMS group, we encountered 36/396 cases
(9.1%) of migration in our study. Duodenal migration
accounted for 27 of these cases (6.8%). This is in the range
of what has been reported previously [15, 23, 27, 28]. We
also report, however, nine cases (2.3%) of proximal
migration of the PCMS. This is likely related to the fore-
shortening of the PCMS with mucosal overgrowth through
the uncovered portion of the SEMS, as previously inves-
tigated by our group [17]. Although this is a less common
mode of migration and less frequently reported by other
investigators, its endoscopic management is more chal-
lenging and requires the combination of balloon dilation
and rat tooth extraction (Figs. 1, 2, 3, 4, and 5). The mean
time to revision was 164 and 90 days for duodenal and
proximal migrations, respectively. All migration cases
were managed with endoscopic removal of the PCMS
except in three cases with malignancy undergoing place-
ment of a PCMS within the previously placed PCMS.
Inability to remove the PCMS is unusual in expert hands
but can be encountered when the PCMS has been in place
for more than 6 months [17] or when access to the mal-
functioning PCMS is precluded by malignancy, as
experienced in the three above patients.
Occlusion rates of PCMS have been reported between
5% and 14% at 6 to 12 months in distal malignant biliary
obstruction [24–29]. In our study population, we found that
occlusion occurred in only 3/396 (0.8%) cases throughout
our follow-up period of 70 months. In malignancy, we
describe occlusion as a separate event from tumor over-
growth: that is, stent clogging may occur separately from
tumor overgrowth through the stent interstices of the
uncovered portions. It has been hypothesized that tumor
burden may promote the formation of biliary sludge and
debris, thereby leading to occlusion via the accumulation of
these particles rather than tumor spread [26]. In cases of
benign biliary disease, in contrast, adherence of bacteria to
the coating membrane has been thought to result in stent
clogging [8, 30, 31]. Interestingly, all our patients with stent
occlusion resulting from debris had a malignant indication.
We did not find tumor in-growth or tumor extension
through the stent to be a complication. Tumor in-growth
through PCMS is regarded as a failure in the covering
membrane and has been described elsewhere [32]. Overall,
the reduced rates of tumor overgrowth in our study com-
pared to uncovered stents for the treatment of distal
malignant biliary obstruction is consistent with other
established studies [16].
Stricture in the uncovered portion of the PCMS in
benign disease occurred in three cases in our study. This is
less frequent than the study published by Cantu et al. that
cited a higher, late complication rate [25]. That group,
however, included only patients with common bile duct
stricture secondary to chronic pancreatitis, known to be a
more difficult group to treat, and only removed PCMS once
malfunction was observed.
Cholecystitis was the second leading complication in
our study. We report an overall rate of 13/396 (3.3%). Prior
studies have suggested that PCMS may be more likely to
cause cholecystitis than uncovered SEMS, specifically
when the covering material overlaps the orifice of the
Fig. 6 Mucosal hyperplasia at the hilum induced by the uncovered
portion of a previously placed PCMS
520 Dig Dis Sci (2010) 55:516–522
123
cystic duct. This is felt to be due to the decreased perme-
ability of PCMS and obstruction to bile flow, when directly
opposed to the cystic duct [17, 26, 33]. The reported rates
of cholecystitis after PCMS placement are between 2.9%
and 12% [26, 29, 34]. We hypothesize that our relatively
low rate of cholecystitis may be related to our systematic
efforts to avoid covering the cystic duct insertion in benign
diseases and to our attempt to irrigate the gallbladder
during ERCP when it was distended before PCMS place-
ment in malignant diseases [12, 17]. Isayama et al. reported
that cholecystitis occurred mainly in patients with tumor
involving the orifice of the cystic duct in the setting of
unresectable distal biliary malignancy [19]. Occlusion of
the cystic duct by tumor was also found to be the major risk
factor for cholecystitis by Suk et al. [18]. Their study found
that 9/15, or 67%, of patients with cholecystitis had cystic
duct involvement by tumor. Another study used intraductal
ultrasonography to diagnose cystic duct invasion by tumor
and found this to be predictive of cholecystitis [23].
In our study, cholecystitis was found in the setting of
tumor involvement in only 2/13 (15%) cases, despite the
finding that 11/13 (85%) patients who developed chole-
cystitis carried primary diagnoses of malignant biliary
disease. This is quite different from rates cited by other
studies [35]. Indeed, in 8/13 (62%) cases of cholecystitis
we report, the cystic duct was covered by our PCMS,
arguing for the positioning of the PCMS as a more
important risk factor.
On the other hand, since 3/13 (23%) cases of cholecys-
titis (at 20, 47, and 55 days after insertion) occurred while
the stent was placed below the cystic duct, other factors
must play a role, such as bacterial colonization after biliary
sphincterotomy, gallstone disease, or perhaps contrast
injection, as previously suggested in the literature [35–38].
Four patients (1%) developed acute pancreatitis or
worsening pancreatitis after PCMS placement. There were
two patients with chronic pancreatitis, one with ampullary
adenoma, and one with benign biliary stricture. One patient
with chronic pancreatitis developed an infected pseudocyst
4 days after PCMS placement for biliary stricture. The
infected pseudocyst occurred in the setting of the PCMS
covering the PD orifice. This patient required removal of the
PCMS and transpapillary drainage. In the patient with
benign biliary stricture, ERCP revealed poor pancreatic duct
drainage likely contributing to the complication of pancre-
atitis. The patient with ampullary adenoma underwent
ampullary resection with biliary and pancreatic sphincter-
otomy and likely developed post-procedure pancreatitis.
We observed two cases of abdominal pain complicating
PCMS placement, both placed in appropriate position
without obstruction. Our study also revealed one case of
liver abscess and one infected biloma after cholecystec-
tomy in a patient with pancreatic cancer; both required
drainage. We believe neither of these complications was
directly related to the PCMS placement.
The present series of patients with PCMS complications
and their management is the largest reported from a single
center to our knowledge. The efficacy of PCMS must be
weighed against their potential complications and their
specific management. Further improvements in the struc-
ture and composition of PCMS are required to prevent
these complications. Indeed, fully covered stents might be
the best option to decrease tumor overgrowth, but also to
prevent mucosal hyperplasia at the proximal portion of the
SEMS. Fenestration of the covered stent at the level of the
cystic duct insertion might prevent cholecystitis. With
newer covered SEMS offering those options arriving on
the market, further multicenter studies should be per-
formed to determine if better efficacy and lower morbidity
can be achieved in both benign and malignant biliary
diseases.
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