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Repeated balloon dilatation with long-term biliary
drainage for treatment of benign biliary-enteric
anastomosis strictures
A STROBE-compliant article
Teng-Fei Li, MD, PhD
a,b
, Pei-Ji Fu, MD, PhD
a,b
, Xin-Wei Han, MD, PhD
a,b,∗
, Ji Ma, MD, PhD
a,b
,
Ming Zhu, MD, PhD
a,b
, Zhen Li, MD, PhD
a,b
, Jian-Zhuang Ren, MD, PhD
a,b
Abstract
Percutaneous balloon dilatation for benign biliary-enteric anastomosis stricture has been the most widely used alternative to
endoscopic treatment. However, patency results from the precedent literature are inconsistent.
The objective of this study was to evaluate the safety and feasibility of repeated balloon dilatation with long-term biliary drainage for
the treatment of benign biliary-enteric anastomosis strictures.
Data from patients with benign biliary-enteric anastomosis strictures who underwent percutaneous transhepatic cholangiography
(PTC), repeated balloon dilatation with long-term biliary drainage (repeated-dilatation group; n =23), or PTC and single balloon
dilatation with long-term biliary drainage (single-dilatation group; n =26) were reviewed. Postoperative complications, jaundice
remission, and sustained anastomosis patency were compared between the groups.
All procedures were successful. No severe intraoperative complications, such as biliary bleeding and perforation, were observed.
The jaundice remission rate in the first week was similar in the 2 groups. During the 26-month follow-up period, 3 patients in the
repeated-dilatation group had recurrences (mean time to recurrence: 22.84 ±0.67 months, range: 18–26 months). In the single-
dilatation group, 15 patients had recurrences (mean time to recurrence =15.28 ±1.63 months, range: 3–18 months). The duration of
patency after dilatation was significantly better in the repeated-dilatation group (P=.01). All patients with recurrence underwent
repeat PTC followed by balloon dilatation and biliary drainage.
Repeated balloon dilatation and biliary drainage is an effective, minimally invasive, and safe procedure for treating benign biliary-
enteric anastomosis strictures, and provides significantly higher patency rates than single dilatation.
Abbreviations: BEA =biliary-enteric anastomosis, MRCP =magnetic resonance cholangiopancreatography, PTC =
percutaneous transhepatic cholangiography, PTCB =percutaneous transhepatic cholangiobiopsy.
Keywords: anastomosis strictures, balloon dilatation, benign
1. Introduction
Anastomotic stricture is a relatively common complication of
biliary-enteric anastomosis (BEA), with a reported incidence of
between 2.6% and 30%.
[1,2]
Strictures may lead to biliary
infection, jaundice, hepatolithiasis, or biliary cirrhosis and can be
associated with significant pain and even death. Surgical revision
of these strictures can be difficult and is associated with both a
significant morbidity rate of approximately 25% and a mortality
rate of between 2% and 13%.
[3,4]
Revisions can further be
associated with increased hospital inpatient stays.
[3,4]
Benign
biliary strictures are commonly managed via an endoscopic
approach. Surgically altered anatomy is not considered as a
contraindication for endoscopy; however, endoscopy is difficult
to perform and is not feasible in some cases.
[5,6]
Percutaneous
transhepatic methods, including percutaneous transhepatic
balloon dilatation with or without biliary drainage, have been
recommended as potential alternatives to an endoscopic
approach. However, the primary patency rates at 24 to 36
months have varied from 62% to 83% in different studies.
[7–10]
A
number of technical aspects of balloon dilatation remains
controversial, for example, the size and length of balloon, the
frequency of dilatation, and the intra-balloon pressure during
dilatation.
[8,11]
In this retrospective study, we compared repeated
balloon with single balloon dilatation, both with biliary drainage.
The primary objective of this study was to determine the safety,
Editor: Bülent Kantarçeken.
TFL and PJF have contributed equally to this work and share the co-first
authorship.
This work was supported by the National Natural Science Foundation of China
(grant number 81801806) and the Technological Research Project of Henan
Provincial Science and Technology Department (grant number 172102310397).
The authors have no conflicts of interest to disclose.
The datasets generated during and/or analyzed during the current study are
available from the corresponding author on reasonable request.
a
Department of Interventional Radiology, the First Affiliated Hospital of
Zhengzhou University,
b
Interventional Institute of Zhengzhou University,
Zhengzhou, China.
∗
Correspondence: Xin-Wei Han, Zhengzhou University, Zhengzhou, Henan,
China (e-mail: xinwei_han@163.com).
Copyright ©2020 the Author(s). Published by Wolters Kluwer Health, Inc.
This is an open access article distributed under the terms of the Creative
Commons Attribution-Non Commercial License 4.0 (CCBY-NC), where it is
permissible to download, share, remix, transform, and buildup the work provided
it is properly cited. The work cannot be used commercially without permission
from the journal.
How to cite this article: Li TF, Fu PJ, Han XW, Ma J, Zhu M, Li Z, Ren JZ.
Repeated balloon dilatation with long-term biliary drainage for treatment of
benign biliary-enteric anastomosis strictures: a STROBE-compliant article.
Medicine 2020;99:44(e22741).
Received: 2 July 2019 / Received in final form: 2 August 2020 / Accepted: 15
September 2020
http://dx.doi.org/10.1097/MD.0000000000022741
Observational Study Medicine®
OPEN
1
feasibility, and long-term efficacy of repeated balloon dilatation
with biliary drainage for benign anastomotic stenosis following
BEA. Secondary study objectives were to evaluate long-term
anastomosis patency and determine the rates of stricture
recurrence following clinically successful balloon dilatation.
2. Materials and methods
2.1. Ethics statement
This retrospective study was approved by the Ethics Committee
of Biomedical Research of Zhengzhou University. All procedures
were in accordance with the 1975 Helsinki Declaration, as
revised in 1983, and written informed consent was obtained from
patients before the performance of each procedure.
2.2. Subject selection
All patients (n =389) who had undergone BEA in our hospital
between January 2016 and Oct 2017 for treatment of
anastomosis strictures were identified by a review of their case
records. Patients were included if they had a benign stricture
(confirmed by forceps biopsy of the stenosis or imaging
examination); were treated by interventional therapy (balloon
dilatation, drainage, and stenting); and had not undergone
previous balloon dilatation or stenting. Patients were excluded if
they had a malignant stricture; had intractable severe blood
coagulation dysfunction; or refused to participate in the study.
Finally, 49 patients who met these criteria were enrolled. These
patients were treated with repeated balloon dilatation with long-
term biliary drainage (repeated-dilatation group; n =23) or single
balloon dilatation with long-term biliary drainage (single-
dilatation group; n=26). All procedures were performed via
the transhepatic approach. Before the procedure, the expected
curative effect and the risks and cost of the 2 treatments were
explained to the patients and/or families and the treatment
approach was decided by them. Among these patients, abdominal
pain, fever, chills, jaundice, and/or pruritus occurred 2 to 5
months after BEA. Prior to dilatation, patients underwent either
diagnostic ultrasonography (n =49), computed tomography (CT)
(n =43), magnetic resonance cholangiopancreatography
(MRCP) (n =44), and/or percutaneous transhepatic cholangio-
biopsy (PTCB) (n =23). The patients’demographics and clinical
characteristics are summarized in Table 1.
2.3. Surgical procedures
All procedures were performed under local anesthesia and
conscious sedation with midazolam (Suzhou Enhua Pharmacy
Co. Ltd., Suzhou, China) by 2 interventional radiologists (TFL
Table 1
Patient demographics and clinical characteristics.
Repeated-dilatation group (n =23) Single-dilatation group (n =26)
Gender
Male 16 14
Female 7 12
Median age, y 50.6 ±13.4 (34–67) 52.3 ±14.3 (34–69)
Clinical manifestations
Abdominal pain 10 11
Fever 7 9
Chills 6 7
Jaundice 19 22
Pruritus 7 11
Serum biochemistry before PTC
∗
ALT, IU/L 229.3 ±144.7 (27–771) 217.4 ±137.4 (27–613)
AST, IU/L 183.7 ±117.3 (25–567) 180.3±107.9 (22–487)
ALP, IU/L 389.9 ±179.2 (120–922) 377.2 ±164.5 (50–948)
Direct bilirubin, mmol/L 125.2 ±104.0 (12.7–334.6) 140.5 ±87.2 (10.3–317.5)
Total bilirubin, mmol/L 93.9 ±81.9 (6.1–255.0) 106.3 ±66.9 (7.1–226.9)
INR 1.1±0.3 (0.6–1.7) 1.1 ±0.3 (0.6–1.7)
Platelet count, 10
9
/L 185.0 ±57.6 (89.0–342.0) 178.1 ±57.7 (87.0–341.0)
Primary disease
Neoplastic diseases 12 14
Cholangiocarcinoma 7 8
Ampullary carcinoma 2 3
Gall bladder carcinoma 3 3
Non-neoplastic diseases 11 12
Iatrogenic bile duct injury (IBDI) 3 4
Choledocholithiasis 5 6
Choledochocele 1 2
Others 2 0
Initial operation
Choledochoduodenostomy 2 3
Choledochojejunostomy 10 9
Hepaticojejunostomy 11 14
∗
PTC =percutaneous transhepatic cholangiography; ALT=alanine aminotransferase; AST =aspartate aminotransferase; ALP =alkaline phosphatase; INR =international normalized ratio.
Li et al. Medicine (2020) 99:44 Medicine
2
and HFY, with 12 and 10 years of experience, respectively).
Based on the MR/MRCP and CT images, PTC was performed
under fluoroscopic guidance, using a 21G Chiba needle (Cook,
Bloomington, IN) from the dilated right and/or left bile duct. PTC
was performed by the standard micropuncture technique. For the
first dilatation, a stiff guidewire (Cook, Bloomington, IN) was
inserted through the strictured section until it reached the
intestinal tract. A 7F catheter sheath (Cook, Bloomington, IN)
was then advanced along the stiff guidewire until the tip was
positioned above the stricture. Cholangiography was repeated to
qualitatively assess the area of stricture through a 5F Cobra
catheter. The catheter was introduced through the sheath and
placed beside the stiff guidewire, with its tip above the stricture.
Then an 8- to 12-mm balloon (Bard Peripheral Vascular, Inc.,
Tempe, AZ) was placed at the level of the diseased section, with
the diameter tailored to both the location and size of the stricture
as appropriate. For example, if the stricture was in an
intrahepatic duct, an 8-mm balloon was used at the first
dilatation. If the stricture was in the extrahepatic duct, such as at
the site of a choledochoduodenostomy, partial choledochojeju-
nostomy, or hepaticojejunostomy, a 10- to 12-mm balloon was
chosen for the first dilatation. Stricture dilatation was achieved
through inflating the balloon to a pressure of between 6 and 8 kPa
and this pressure was maintained for 3 to 5 minutes. After ≥3
minutes, the dilatation process was repeated at least once. If the
contrast agent was observed to smoothly pass through the
original stricture point into the distal intestine, an 8.5F to 10.2F
internal and external biliary drainage tube (Cook, Bloomington,
IN) was placed (Fig. 1A–H). This procedure was repeated every
month for the first 3 months following the first intervention, and
then every 2 months until the biliary drainage tube was removed
at the end of 6 months. Over these 6 months the dilatation had
been conducted a total of 5 times (Fig. 2). After each procedure
vital signs were monitored and abdominal signs and symptoms
including rigors, fever, vomiting, and abdominal pain were
recorded. In addition, the nature and volume of fluid drainage
were documented. The indication for removing the drainage tube
is based on a consideration of hepatic and renal function,
abdomen ultrasound, MRCP, and/or radiography. In the
presence of abnormal clinical parameters, the drainage tube
was left in situ and additional dilatation was performed if
necessary. Patients in the single-dilatation group underwent only
balloon dilatation and biliary drainage, and the tube was
removed 6 months later. The balloon type used and technique
applied were the same as those used in the repeated-dilatation
group.
2.4. Efficacy evaluation, follow-up, and definitions
Patients were administered prophylactic antibiotics and symp-
tomatic treatment as required postoperatively. One week
following the dilatation procedure, patients were examined for
remission of jaundice and any short-term complications
associated with the dilatation procedure. Serum bilirubin
concentration was monitored 1 week after the procedure.
Following removal of the tube, anastomosis patency and patient
survival were assessed via follow-up outpatient visits or
telephone interview every month as required. Clinical success
of the dilatation procedure was defined radiologically as a <30%
residual narrowing at the biliary-enteric anastomosis relative to
bile duct caliber as measured from the cranial aspect of the
anastomosis on either contrast CT, magnetic resonance imaging
Figure 1. A case of benign anastomotic stricture treated with repeated balloon dilatation with long-term biliary drainage. (A–C) This figure depicts a 26-year-old
woman who underwent cholecystectomy, cholangiolithotomy, and hepaticojejunostomy for cholecystocholedo-cholithiasis 6 months previously. Four months
following this procedure she presented with abdominal distension and fever. CT and PTC revealed a benign biliary-enteric anastomosis stricture. (D–E) Balloon
dilatations were performed in the right and left bile ducts. (F) Post balloon dilatation, 2 8.5F internal and external biliary drainage tubes were implanted at each side.
(G) At 6 months postoperatively, CT showed no obvious dilatation of the intrahepatic bile ducts. (H) Repeat biliary angiography showed that the narrowing was
cleared, following which the drainage tubes were removed. CT =computed tomography; PTC =percutaneous transhepatic cholangiography.
Li et al. Medicine (2020) 99:44 www.md-journal.com
3
(MRI), or ultrasound. Normalization of previously elevated
serum bilirubin, pruritus remission (if present), and resolution of
other related clinical symptoms were required prior to drainage
tubes being removed. Recurrence was defined as the re-
development of clinically significant symptoms suggesting re-
stenosis such as jaundice and cholangitis, subsequently necessi-
tating intervention. In practice, stricture recurrence was diag-
nosed based on a combination of clinical symptomatology, serum
biochemical tests, and imaging examination.
2.5. Statistical analysis
Biochemical indices were summarized as mean ±SD and
compared using the Wilcoxon signed-rank test. Categorical data
were analyzed using the Chi-squared or Fisher exact test in the
case of small numbers. Anastomosis patency duration and
survival rates were compared using the Kaplan–Meier method.
For all analyses P<.05 was considered significant. All statistical
analyses were performed using SPSS for Windows, version 19.0
(IBM Corp., Armonk, NY).
3. Results
3.1. Complications and management
Dilatation procedures were successfully performed in all patients.
In order to image the stricture, bilateral PTC was performed in 16
of the repeated-dilatation group patients with the remaining 7
undergoing unilateral PTC. Similarly, bilateral and unilateral
PTC was used in 17 and 9 single-dilatation patients respectively.
No electrocardiographic abnormality was observed in either
group during the intervention. Across both groups no bile duct
perforation, peri-biliary sepsis, or hemorrhage occurred intra-
operatively. Postoperatively, 3 patients in the repeated-dilatation
Figure 2. Schematic diagram of our treatment protocol.
Li et al. Medicine (2020) 99:44 Medicine
4
group and 4 patients in the single-dilatation group subsequently
presented with symptoms of cholangitis including abdominal
pain, chills, and fever. These resolved with antibiotics and
conservative management. Repeat routine blood tests following
symptomatic management confirmed all laboratory markers had
returned to baseline in these patients.
3.2. Outcomes and follow-up
In both groups, predilatation abdominal distension/pain, fever,
chills, pruritus, and loss of appetite were almost completely
resolved. There was no difference between surgical groups in
either total or direct bilirubin levels at 1-week following the
procedure (Table 2).
During the 26-month follow-up period, 3 patients in the
repeated-dilatation group had recurrences (mean time to
recurrence: 22.84 ±0.67 months, range: 18–26 months), while
15 patients in the single-dilatation group had recurrences (mean
time to recurrence: 15.28 ±1.63 months, range: 3–18 months).
The difference between the groups with regard to the time to
recurrence was statistically significant (P=.01; Fig. 3).
In the repeated-dilatation group, jaundice recurred in 1 patient
at 11 months after the procedure (total bilirubin level: 116 mmol/
L, direct bilirubin level: 87 mmol/L). Additionally, 1 patient had
recurrent infection at posttreatment 15 months and 1 patient was
febrile at 19 months after the procedure. Stricture was confirmed
by enhanced CT or ultrasound and treated by repeat balloon
dilatation. In the single-dilatation group, there were 15
recurrences. One of these patients had disseminated intravascular
coagulation and biliary sepsis secondary to recurrent jaundice
and died 3.2 months after balloon dilatation. The other 14
patients improved after repeat dilatations.
4. Discussion
Biliary-enteric anastomosis stricture is a major complication
associated with hepatobiliary surgery. Approximately 20% of
the strictures occur within 6 months of surgery.
[12]
The leading
causes of benign biliary stricture include intraoperative injury,
trauma, cholangitis associated with choledocholithiasis, hepatic
artery ischemia, and sclerosing cholangitis. To date, the accepted
first-line management of benign biliary strictures is endoscopic
resolution. However, an endoscopic approach is generally
considered to be inappropriate in patients who have previously
undergone bilioenterostomy.
[5,6]
In such situations, per-oral
cholangioscopy-assisted antegrade intervention has been
reported as a useful technique. In addition, other novel
alternative interventional EUS techniques have been also
reported, such as EUS-directed transgastric ERCP in patients
with Roux-en-Y gastric bypass.
[13,14]
Novel devices and tools
designed for EUS-guided transluminal interventions allow
various new applications and improve the efficacy and safety
of these procedures. Specially designed stents and stent insertion
devices enable intra- and extra-hepatic bile stenting as well as
Table 2
Decrease in total bilirubin levels and direct bilirubin levels in the 2 study groups (mmol/L).
Total bilirubin levels Direct bilirubin levels
Group Before intervention After intervention D-value PBefore intervention After intervention D-value P
Repeated-dilatation group (n =23) 125.2 ±104.0 54.5 ±47.6 70.7 ±65.1 .82 93.9 ±81.9 36.6 ±34.4 57.3 ±53.8 .92
Single-dilatation group (n =26) 140.5 ±87.2 65.9 ±42.0 74.6 ±51.3 106.3 ±66.9 50.3 ±33.5 56.0 ±39.8
Figure 3. Kaplan–Meier plot of probability of 2 groups having clinically significant restenosis.
Li et al. Medicine (2020) 99:44 www.md-journal.com
5
gallbladder drainage.
[15,16]
However, as it relies extremely on
experience of the operator, EUS-guided transluminal interven-
tions are restricted in the clinical application. Although the
transhepatic approach is invasive, in some difficult cases,
percutaneous transhepatic surgical approaches, including percu-
taneous transhepatic balloon dilatation with or without long-
term biliary drainage and stent placement, have been suggested as
possible alternatives.
[5,6,17]
The appropriate placement of a stent
to take advantage of both the increased expansive force and
prolonged dilatation effect of an in-situ stent may be associated
with an increased success rate for the treatment of benign biliary
strictures. Placement of non-retrievable, uncovered metallic
stents have previously been attempted in patients with refractory
benign biliary strictures.
[18–20]
However, low long-term patency
and difficulty removing these stents secondary to hyperplastic
tissue in-growth have limited its clinical use.
[19,20]
The recently
developed covered metallic stents may be better for maintaining
mid- to long-term patency, and, in addition, they are easier to
remove.
[21–25]
However, in contrast to uncovered devices,
covered metallic stents do not integrate into the surrounding
tissue and this may in turn be associated with higher migration
rates away from their original insertion location. Previous studies
of covered stent placement for benign biliary strictures have
reported an incidence of stent migration ranging from 2.8% to
25%.
[21–25]
Biodegradable stents are increasingly being used in
the heart and other areas to provide adequate support for
stenosis. As these stents degrade completely, the complications
associated with stenting are reduced. Although the treatment of
benign biliary strictures is still in its initial stages, the use of these
stents is an important direction for the future.
[26,27]
To date, percutaneous balloon dilatation of benign biliary-enteric
anastomosis strictures has been the most widely used alternative to
endoscopic treatment.
[28–31]
However, patency results from the
precedent literature are inconsistent.
[28–31]
In this study, we found
that repeated balloon dilatation with long-term biliary drainage was
associated with significantly greater long-term anastomosis patency
relative to patients undergoing single dilatation. Schwarzenberg
et al
[32]
reported that repeated procedures conducted at 2- to 3-week
intervals in 3 patients was associated with persistent biliary patency
over a median 6.5 months of follow-up. Luo et al
[33]
reported that
the anastomosis site could be progressively dilated via a balloon left
in situ for up to 3 months following surgery; they found that the
stricture did not recur, probably because of the support provided by
the balloon during the period of wound healing and tissue
remodeling at the site of anastomosis. This is consistent with what
is known about the final phase of wound healing and scar tissue
formation. Broughton reported that wound strength never returns to
100%; from 3% at 1 week to 30% at 3 weeks 30% and
approximately 80% after 3 months.
[34]
The optimal timing for removing drainage tubes post dilatation
is complex and difficult to define. In this study, the biliary long-
term drain was left in place after balloon dilatation not only to
provide drainage but also for mechanical support of the dilated
stricture and for performance of follow-up cholangiography to
identify restenosis. If the anastomotic stenosis does not recur
within 6 months of the index dilatation, the drain is removed.
Some investigators have reported performing percutaneous
transhepatic large-diameter (up to 20-F) tube interpositions
through the benign bilioenterostomy stricture with long-term
drainage.
[13]
However, the long-term maintenance of Percutane-
ous transhepatic biliary drainage catheters can result in
significant patient discomfort and/or an increased risk of
infection.
[6]
Other surgeons may be more interested in functional
or clinical outcomes and end-points. If the patient tolerates the
external biliary drain with cap for 1 to 2 weeks, the drain is
subsequently removed entirely. Surgeons who prioritize clinical
outcomes may lead to patients being asymptomatic for months
after an anastomotic stricture has recurred.
[35]
Despite stricture
recurrence, this approach may be associated with an extended
period where the patient is “tube-free,”an important morbidity
consideration for patients. This potential trade-off between
prioritizing patient comfort and maximizing patency duration
may underscore, at least in part, the wide discrepancy in patency
data in balloon dilatation studies. Clinicians who prioritize
functional/clinical outcomes tend to report superior patency than
those that rely solely on anatomical/cholangiographic outcomes.
Our study has several limitations. First, this was a retrospective
study, and a selection bias may be present. Prospective,
randomized trials would be required to validate our findings
and better control for various imbalances in the distribution of
prognostic correlates of our study end-points between treatment
groups. Further, there is possibility that our outcome data is
incomplete, for example, in patients who developed complications
after balloon dilatation, but did not return to our institution for
follow-up. However the likelihood of these scenarios are low, as all
patients in our study residedlocally and were likely to return to the
care of their hepatobiliary surgeon in case of a complication.
In conclusion, our findings suggest that repeated balloon
dilatation with long-term biliary drainage of biliary-enteric
anastomosis strictures may provide a lasting benefit and can
prevent the need for a surgical revision of the anastomosis,
relative to patients undergoing single dilatation. We recommend
that repeated balloon dilatation with long-term biliary drainage
should be considered in patients with biliary-enteric anastomotic
strictures, who are otherwise inappropriate for endoscopic
management.
Author contributions
Conceptualization: Teng-Fei Li, Pei-Ji Fu, Xinwei Han, Ji Ma,
Ming Zhu.
Data curation: Teng-Fei Li, Pei-Ji Fu, Xinwei Han, Zhen Li, Jian-
Zhuang Ren.
Formal analysis: Teng-Fei Li, Pei-Ji Fu, Xinwei Han, Ji Ma, Ming
Zhu, Jian-Zhuang Ren.
Funding acquisition: Xinwei Han.
Investigation: Teng-Fei Li, Pei-Ji Fu, Xinwei Han, Ming Zhu,
Zhen Li, Jian-Zhuang Ren.
Methodology: Teng-Fei Li, Pei-Ji Fu, Xinwei Han, Ji Ma, Ming
Zhu, Jian-Zhuang Ren.
Project administration: Teng-Fei Li, Pei-Ji Fu, Xinwei Han, Ji Ma,
Jian-Zhuang Ren.
Supervision: Teng-Fei Li, Pei-Ji Fu, Xinwei Han, Ji Ma, Ming
Zhu, Zhen Li, Jian-Zhuang Ren.
Validation: Teng-Fei Li, Pei-Ji Fu, Xinwei Han, Ming Zhu.
Visualization: Teng-Fei Li, Pei-Ji Fu, Xinwei Han.
Writing –original draft: Teng-Fei Li, Pei-Ji Fu, Xinwei Han.
Writing –review & editing: Teng-Fei Li, Pei-Ji Fu, Xinwei Han, Ji
Ma, Zhen Li.
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