ORIGINAL ARTICLE: Clinical Endoscopy

Endotherapy of postoperative biliary strictures with multiple stents:

results after more than 10 years of follow-up
Guido Costamagna, MD, FACG, Andrea Tringali, MD, PhD, Massimiliano Mutignani, MD, Vincenzo Perri, MD,
Cristiano Spada, MD, Monica Pandolfi, MD, Domenico Galasso, MD
Rome, Italy

Background: Endoscopic dilation of postoperative biliary strictures with increasing numbers of stents was first
described by our group in 2001 with promising results after a long-term follow-up (mean 4 years).
Objective: To verify results of endoscopic treatment of postoperative biliary strictures at a very-long-term
follow-up.
Design: Single center, follow-up study.
Setting: Tertiary-care, academic referral center.
Patients: A group of 42 patients from our 2001 study, who had undergone endoscopic dilation of postoperative
biliary strictures with the multiple endoscopic stenting technique, underwent systematic follow-up. The last
telephone follow-up was done in September 2009.
Intervention: Clinical conditions and the occurrence of new biliary symptoms during the follow-up period were
assessed, and results of the most recent liver function tests and abdominal US were recovered.
Main Outcome Measurements: Occurrence of cholangitis and liver function test evaluation during the
follow-up period.
Results: Of the 40 patients who were alive at the end of the study published in 2001, 5 (12.5%) died of unrelated
causes after a mean of 6.7 years (range 3-13.3 years) from the end of treatment, without further biliary symptoms.
The overall mean follow-up time for the remaining 35 patients (87.5%) was 13.7 years (range 11.7-19.8 years).
Seven patients (20%) experienced recurrent acute cholangitis after a mean of 6.8 years (range 3.1-11.7 years) from
the end of treatment. All 7 of these patients underwent ERCP. Four of the 7 patients had postoperative biliary
stricture recurrence (n ⫽ 4/35, 11.4%) that was retreated endoscopically with placement of stents, and the other
3 patients had common bile duct stones (n ⫽ 3/35, 8.6%) that were extracted. No stricture or bile duct stone
recurrences after retreatment were recorded after a mean follow-up period of a further 7.1 years (range 2.5-12.1
years). Twenty-eight patients remained asymptomatic with normal liver function test results and abdominal US
results after a mean follow-up period of 13.7 years (range 11.7-19.8 years).
Limitations: Telephone follow-up.
Conclusion: Results of multiple endoscopic stenting for postoperative biliary strictures remain excellent even
after a very-long-term follow-up. The stricture recurrence rate is low, and recurrences can be retreated
endoscopically. (Gastrointest Endosc 2010;72:551-7.)

Abbreviation: POBS, postoperative biliary strictures.
DISCLOSURE: All authors disclosed no financial relationships relevant to
this publication.
See CME section; p. 600
Copyright © 2010 by the American Society for Gastrointestinal Endoscopy
0016-5107/$36.00
doi:10.1016/j.gie.2010.04.052
Received January 11, 2010. Accepted April 29, 2010.
Current affiliations: Digestive Endoscopy Unit (G.C., A.T., M.M., V.P., C.S.,
D.G.), Catholic University, Digestive Diseases Department (M.P.), Campus
Bio-Medico University, Rome, Italy.
Reprint requests: Professor Guido Costamagna, Head of Digestive
Endoscopy Unit, Catholic University, Largo A. Gemelli 8, 00168 Rome, Italy.
If you would like to chat with an author of this article, you may contact Dr
Costamagna at gcostamagna@rm.unicatt.it.

www.giejournal.org Volume 72, No. 3 : 2010 GASTROINTESTINAL ENDOSCOPY 551

Endotherapy of postoperative biliary strictures
Endoscopic management of postoperative biliary stric-
tures (POBS), by placement of an increasing number of
stents until complete morphologic disappearance of the
stricture is achieved, was introduced in 20011 with prom-
ising results after a long-term follow-up period (mean 4
years). These promising results were confirmed by other
studies that used this aggressive approach for POBS2 and
other benign biliary strictures, such as those arising in the
course of chronic pancreatitis.3-5
In the following years, the “historical” group of 42
patients treated for POBS1 with this novel approach un-
derwent systematic clinical and instrumental follow-up
after the end of treatment. Results of the very-long-term
follow-up are reported here.
PATIENTS AND METHODS
The study group consisted of 42 patients1 who under-
went aggressive endoscopic treatment of POBS by use of
an increasing number of large-bore plastic stents between
December 1987 and December 1997. POBS were classified
according to the Bismuth and Lazorthes6 method: 36% had
type I strictures, 21% type II, 17% type III, 19% type IV, and
7% type V.
The 42 patients underwent systematic follow-up: all
were asked to undergo liver function tests (total and direct
bilirubin, aspartate aminotransferase, alanine aminotrans-
ferase, alkaline phosphatase, and gamma glutamyl trans-
ferase) and transabdominal US every 6 months from the
end of treatment, and a telephone interview was done
yearly to assess the occurrence of cholangitis and to eval-
uate the results of liver function tests and US: these study
endpoints were consistent throughout the study period
starting from the first series. During the yearly follow-up,
patients were asked to provide us with the reports of liver
function tests and US.
In case of cholangitis or evidence of abnormal liver
function tests on repeated samples or bile duct dilation on
US, an ERCP was performed by the same endoscopists
(G.C., M.M., V.P.) involved in the 2001 study. In case of
POBS recurrence, the maximum number of plastic stents
were reinserted according to stricture tightness and bile
duct diameter; elective stent exchange was planned at
3-month intervals, and the presence or absence of the
stricture was assessed by occlusion cholangiograms. Stents
were reinserted until complete morphologic stricture res-
olution was observed. The first study1 was not submitted
for internal review board approval because, at that time,
the ethics committee of our hospital did not require noti-
fication for retrospective studies. The current study is a
continuation of the follow-up of the initial study. Patients
were informed about the retrospective study when con-
tacted by telephone for the follow-up interviews. All pa-
tients provided oral consent for us to publish the results of
laboratory test findings communicated during the inter-
views, with their names withheld.
552 GASTROINTESTINAL ENDOSCOPY Volume 72, No. 3 : 2010
Costamagna et al
Take-home Message
● This study confirms very good results of endoscopic
treatment of postoperative biliary strictures by insertion
of multiple plastic stents even after a very-long-term
follow-up period (more than 10 years). Stricture
recurrence after endoscopic treatment of postoperative
biliary strictures can be safely and successfully retreated
by ERCP.
Statistical methods
Quantitative data were summarized by the mean, me-
dian, range, and interquartile range (IQR), as appropriate.
The distributions of survival of stent patency over time
were estimated by the Kaplan-Meier product-moment
method. The log rank test was used to compare these
distributions in two groups.
RESULTS
No patients were lost to follow-up. Five patients
(12.5%) died from unrelated causes (thyroid cancer, phar-
ynx cancer, prostate cancer, heart failure, motorbike acci-
dent) after a mean of 6.7 years (range 3-13.3 years, median
6 years, IQR 3-8) from the end of treatment. These patients
did not experience further episodes of cholangitis during
their lives, and the last liver function test results and
abdominal US results were within normal ranges.
The mean follow-up period for the remaining 35 pa-
tients (87.5%) was 13.7 years (range 11.7-19.8 years, me-
dian 13.2 years, IQR 12.4-14.5). The last telephone contact
with these patients was in September 2009, and 25 of the
35 patients (71.4%) sent us the last liver function test
results and/or US results.
Twenty-eight patients (80%) were in good clinical con-
dition, and their liver function test and US results remained
within the normal range after a mean of 13.6 years (range
11.7-19.8 years, median 13.1 years, IQR 12.4-13.7). One of
these patients asked to undergo repeat ERCP to verify the
condition of his bile ducts 7 years after the end of treat-
ment because of legal recourse for a postlaparoscopic
cholecystectomy injury (Fig. 1). The only patient (de-
scribed in the 20011 article) without complete morpho-
logic disappearance of the stricture after 18 months of
stenting is still asymptomatic, with normal liver function
test results after 12.1 years.
Seven patients (20%) experienced further episodes of
cholangitis after a mean follow-up period of 6.8 years
(range 3.1-11.7 years, median 6.6 years, IQR 5-8) from the
end of treatment and underwent repeat ERCP. In 3 of 35
cases (8.6%), recurrence of cholangitis after a mean of 7.6
years (range 3.1-11.7 years, median 7.9 years, IQR 5.5-9.8)
was secondary to newly formed common bile duct stones
(n ⫽ 2) and intrabiliary food residue (vegetables) (n ⫽ 1).
www.giejournal.org
Costamagna et al
Figure 1. A, Cholangiogram at the end of endoscopic treatment of a Bismuth type II benign biliary stricture after laparoscopic cholecystectomy.
B, Seven years later. Arrows are placed at the site of the previous stricture.
Bile duct clearance was successfully achieved by ERCP.
These patients remained asymptomatic after a further
follow-up period of 7.7 years (range 2.5-12.1 years, me-
dian 8.4 years, IQR 5.4-10.2). In 4 of 35 patients (11.4%),
POBS recurrence occurred after a mean of 6.2 years (range
4.4-8.2 years, median 6.1 years, IQR 5.2-7), and all of these
patients asked for endoscopic retreatment.
In one case, stricture recurrence was attributed, after
review of radiographs of the previous treatment, to an
incomplete treatment 12 years earlier. In this case, retreat-
ment achieved a satisfactory, but not complete, resolution
of the stricture despite reinsertion of a maximum of 5
large-bore stents. The treatment was interrupted because
insertion of more stents was considered not feasible and
because of poor compliance of the patient, who had re-
cently diagnosed Parkinson’s disease (Fig. 2). Another
patient had good resolution of the stricture on the com-
mon bile duct, but a stricture of the right posterolateral
duct was discovered (this stricture was not diagnosed at
the first treatment) and was the reason for cholangitis
recurrence. In the third patient, stricture recurrence was
the reason for repeated cholangitis at 7 years from the first
treatment. The fourth case, a patient with a Billroth II
stomach, had recurrence of a stricture of the left hepatic
duct.
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Endotherapy of postoperative biliary strictures
These 4 patients underwent endoscopic retreatment
with the multiple endoscopic stenting technique. No com-
plications (pancreatitis, cholangitis because of stent occlu-
sion, stent displacement) occurred during retreatment. A
mean number of 2.7 ERCPs (range 2-3) were performed,
with reinsertion of a mean number of 4.5 (range 4-5) 10F,
plastic stents. The mean duration of retreatment was 7
months. All of these patients were in good condition, with
normal liver function test results and liver US results after
a mean of 6.7 years (range 3.9-9.7 years, median 6.6 years,
IQR 5.5-7.8) from stent removal after the end of retreat-
ment. No patients had a second stricture or stone recur-
rence after retreatment. A comparison of long- and very-
long follow-up period results is summarized in Table 1.
Kaplan-Meier analysis showed no significant differ-
ences in the bile duct patency rate according to the num-
ber of ERCPs required to treat the postoperative bile duct
strictures. The cut-off of 4 ERCPs was chosen because the
resultant categories appeared to have approximately sim-
ilar rates for the subcategories within (Fig. 3).
DISCUSSION
POBS need a multidisciplinary approach from diagnosis
to treatment. With the advent of laparoscopic cholecystec-
Volume 72, No. 3 : 2010 GASTROINTESTINAL ENDOSCOPY 553
Endotherapy of postoperative biliary strictures Costamagna et al

Figure 2. A, Recurrence of a Bismuth type II benign biliary stricture (arrow) after open cholecystectomy 4 years after the end of endoscopic treatment.
B, Five 10F stents were reinserted. C, Final cholangiogram after retreatment, with good stricture resolution (arrow).

tomy, the incidence of bile duct lesions has increased
significantly.7 Patients with POBS are usually healthy and
young, but this “benign” event can affect quality of life
significantly.8,9
Three kinds of treatment are available: surgical, endo-
scopic, and percutaneous. Surgical treatment of POBS
should be performed in referral hepatobiliary surgical
units because surgical repair may be technically very de-
manding, and long-term results are better in high-volume
centers. The reported mortality of surgical repair is low
(0%-2.2%) but present, and postoperative morbidity
ranges from 9.5% to 42.9% (Table 2).10-21 Long-term results

554 GASTROINTESTINAL ENDOSCOPY Volume 72, No. 3 : 2010 www.giejournal.org

Costamagna et al Endotherapy of postoperative biliary strictures

years) (Table 2); the morbidity and mortality rates after

TABLE 1. Results of previously published,1 long-term reintervention for anastomotic strictures are not reported
follow-up study and most recent very-long-term follow- in detail. Bilioenteric anastomotic strictures require rein-
up results of 42 patients with postoperative biliary
tervention, with its associated morbidity and mortality,10 or
strictures treated with an increasing number of stents
repeated percutaneous dilations,22-25 with impairment of
Follow-up period patients’ quality of life because of the presence of percu-
Long term Very long term
taneous drains for long periods (about 1 year). Results of
Follow-up finding (year 1998) (year 2009) percutaneous dilation of strictured biliodigestive anasto-
Mean follow-up period, 4 (2-11.3) 13.7 (11.7-19.8)
mosis for POBS report a 67% to 80% success rate after a
years (range) mean follow-up period of 3.1 years (range 2-5.2 years).23-26
Percutaneous treatment of POBS in patients without
Patient lost to follow-up 0 0
bilioenteric anastomosis and surgical reconstruction is not
Patient died of 2 5 considered the first-line approach.26 However, interven-
unrelated cause tional radiologists play a key role in the multidisciplinary
Asymptomatic with 39/40 (97.5) 28/35 (80) approach to POBS.21 When ERCP fails to pass a POBS, the
normal LFT, no. (%) percutaneous approach can help in overcoming the stric-
ture and completing the treatment by endoscopy with the
Cholangitis recurrence, 1/40 (2.5) 7/35 (20)
no. (%) rendezvous technique. Furthermore, preoperative percu-
taneous biliary drainage is helpful to the surgeons in cases
Stricture recurrence 0 4/35 (11.4)
of complete transection of the common bile duct to delin-
Stones/food 1 (2.5) 3/35 (8.6) eate the proximal extent of the injury. This is considered
LFT, Liver function test results. part of the surgical procedure.21
Only one published retrospective study27 compared “stan-
dard” endoscopic treatment of POBS (2 stents, with elective
exchange every 3 months for 1 year) with surgery. Early
complications were more common in the surgical group, and
late complications related to stent occlusion were more com-
mon in the endotherapy group. Long-term success rates were
similar in both groups, with recurrent stricturing in 17% of
each group after a mean follow-up period of 4.1 years for
endoscopy and 3.5 years for surgery.
The “standard” endoscopic approach to POBS resulted
in 20% POBS recurrence after a median follow-up period
of 9.1 years.28 All cases of recurrent stenosis occurred
within 2 years of stent removal, as a potential result of an
incomplete treatment.
In our experience, results of the aggressive endoscopic
approach to POBS after a mean follow-up period of 13.7
years are very good, with 80% of patients having excellent
results and an 11.4% stricture recurrence rate after more
Figure 3. Kaplan-Meier plot showing bile duct patency according to the than 6 years from the end of treatment. Furthermore,
number of ERCPs performed.
cholangitis recurrence is not always related to POBS re-
currence but also can be secondary to stone formation, as
of surgical treatment of POBS are classified11,21,22 as excel- occurred in 3 of 7 (43%) of our cases with relapsing
lent (no biliary symptoms, with normal liver function test symptoms.
results), good (transitory biliary symptoms and normal Reading of a retrograde cholangiography at the first
liver function test results or asymptomatic with mildly treatment for POBS can be difficult (ie, due to the presence
elevated liver function test results), fair (biliary symptoms of a T tube or a concomitant biliary leak). This fact might
with abnormal liver function test results), and poor (recur- have been the reason for incomplete treatment discovered
rent strictures requiring further treatment). Excellent and at the time of POBS recurrence in 2 of 4 cases with
good results together are reported in 75.9% to 90.8% of recurrent strictures. These cases were treated in a “pre-
cases, but this figure includes, where reported,11,14,15,19 5% MRCP era;” today, interpretation of cholangiography in
to 21.7% of patients with fluctuating cholestasis (Table 2). case of POBS is more accurate, MRCP being part of the
Furthermore, the reported incidence of long-term stric- preoperative work-up for POBS.
tures of the biliodigestive anastomosis ranges from 6% to The main limitations of endoscopic treatment of POBS
32% after a mean follow-up period of 6 years (range 4-9.5 by the multiple endoscopic stenting method are the need

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Endotherapy of postoperative biliary strictures Costamagna et al

TABLE 2. Results of published series on surgical treatment of benign biliary strictures

Mean Excellent/good Good results Anastomotic

follow-up results during during strictures during
Study No. Morbidity, Mortality, period follow-up follow-up follow-up
First author/year design patients no. (%) no. (%) (years) no. (%) no. (%) no. (%)
Chapman/199510 R 110 NA 2 (1.8) 7.2 79 (75.9) NA 22/108 (20.4)

McDonald/199511 R 45 16 (36) 0 4.6 39 (86.6) 8/39 (20.5) 6/45 (13)

Tocchi/199612 R 84 18 (21.4) 2 (2.2) 9 70 (83.3) NA 10 (12.2)

Röthlin/199813 R 51 17 (33) 1 (2) 7.6 NA NA 3 (6)

14
Murr/1999 R 59 10 (17) 1 (1.7) 3.7 49 (90.7) 3/49 (5) 5/54 (9.3)
15
Lillemoe/2000 P 156 NA 1 (0.6) 4.8 129 (90.8) 28/129 (21.7) 13/142 (9.2)
16
Quintero/2001 R 65 NA 1 (1.5) NA NA NA 6/64 (9.3)
17
Huang/2003 P 25 NA 0 4.5 NA NA 8/25 (32)
18
Sicklick/2005 R 175 75 (42.9) 3 (1.7) NA NA NA NA

Sikora/200619 P 300* 100 (33.3) 4 (1.3) 9.5 134 (90) 12/134 (8) 15/149 (10)

Walsh/200720 R 84 8 (9.5) 1 (1.2) 5.6 NA NA 11/83 (13.2)

Nuzzo/200821 P 41 6 (14.6) 0 4 32 (78) NA 6/41 (14.6)

R, Retrospective; P, prospective; NA, not addressed.
*Follow-up on 149 patients.

for multiple ERCPs and repeated hospitalizations, leading
to high costs and potentially limited patient compliance. In
our experience, after the risks and benefits of the possible
treatments for POBS were explained to the patient, with
the help of the hepatobiliary surgeon, patients asked for
endoscopic treatment and retreatment, if needed.
POBS recurrence can be successfully retreated by
ERCP, which has the advantage of being repeatable with
low associated morbidity in case of a pre-existing sphinc-
terotomy. Recently developed covered and removable
self-expanding metal stents can represent a single-step
endoscopic treatment for POBS, but many limitations29
limit their use for benign diseases. POBS are usually short,
located in the upper third of the common bile duct, and
the bile duct below the stricture is normal. These features
need a careful evaluation of covered and removable metal
stents in the setting of prospective studies to assess results
and complications and define stent characteristics (ie, ma-
terial, radial force, diameter, length). Bioabsorbable biliary
stents are an attractive option, but their use is still under-
going experimental animal evaluation.
In conclusion, endoscopic stenting with the aim of
inserting multiple plastic stents is a reasonable, first-line
approach in the treatment of postsurgical strictures.30
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