Digestive Endoscopy 2017; 29 (Suppl. 2): 88–93 doi: 10.1111/den.

12836

Current status of biliary drainage strategy for acute cholangitis –Endoscopic

treatment for acute cholangitis with common bile duct stone and stent occlusion–

Management of acute cholangitis as a result of occlusion

from a self-expandable metallic stent in patients with
malignant distal and hilar biliary obstructions
Hideyuki Shiomi,1 Kazuya Matsumoto2 and Hiroyuki Isayama3
1
Division of Gastroenterology, Department of Internal Medicine, Graduate School of Medicine, Kobe University,
Kobe, Hyogo, 2Department of Gastroenterology, Tottori University Hospital, Tottori, and 3Department of
Gastroenterology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan

Acute cholangitis as a result of common bile duct stones can be
managed; however, cholangitis caused by occlusion with a
biliary self-expandable metallic stent (SEMS) in patients with an
unresectable malignant biliary obstruction has not been fully
discussed. The acute cholangitis clinical guidelines (Tokyo
Guidelines 2013) recommend following the same procedure
as that used for cholangitis; however, the patient’s condition,
including performance status, tumor extension or staging, and
prognosis must be considered. Most physicians manage
cholangitis from a SEMS occlusion using a two-step procedure.
They insert endoscopic drainage with a plastic stent or insert a
nasobiliary drainage tube, which does not exacerbate sepsis.
Addition or replacement of a biliary SEMS is required in many
cases depending on the cause of the occlusion. Tumor ingrowth
through the stent mesh is common in uncovered SEMS and
requires placement of another stent in an in-stent method.
However, covered SEMS tends to be occluded by sludge, so it
must be replaced because of the bacterial biofilm that forms on
the covering membrane. The location of the biliary stricture
(hilar or distal) should also be considered. Strategies for
managing cholangitis as a result of occlusion by a biliary SEMS
remain controversial, so prospective clinical trials are needed.
Key words: biliary stent, biliary stricture, endoscopic biliary
drainage, obstructive jaundice, self-expandable metallic stent

INTRODUCTION MANAGEMENT OF CHOLANGITIS AS A

M ANAGEMENT OF ACUTE cholangitis as a result of
common bile duct stones has been comprehensively
discussed. However, the appropriate management for acute
cholangitis as a result of an occluded self-expandable
metallic stent (SEMS) remains controversial. Because this is
a common emergency situation, treatment strategies should
be established for this type of cholangitis. Patients who
undergo a SEMS procedure are always in poor physical
condition from an unresectable malignancy with or without
chemotherapy. The treatment strategy can differ depending
on whether a distal or a hilar stricture is causing the stenosis.
In this review, we discuss strategies to treat cholangitis as a
result of a SEMS occlusion.
Corresponding: Hiroyuki Isayama, Department of
Gastroenterology, Graduate School of Medicine, The University
of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan.
Email: isayama-tky@umin.ac.jp
Received 18 December 2016; accepted 2 February 2017.
RESULT OF A SEMS OCCLUSION
A CUTE CHOLANGITIS AS a result of an occluded
SEMS can rapidly progress to a severe stage accom-
panied by organ dysfunction; thus, early detection is
necessary for appropriate management, including emer-
gency biliary drainage and medical treatment. These patients
are advised to seek immediate medical attention when they
have symptoms, such as fever and jaundice. Medical
personnel are also educated to contact experts for immediate
consultation when patients with symptoms call or visit.
Patients with acute cholangitis receive blood biochemical
testing at regular intervals and early stent replacement and
re-drainage should be considered if biliary system enzyme
levels are higher than normal. Furthermore, computed
tomography (CT), magnetic resonance cholangiopancre-
atography (MRCP) and abdominal ultrasonography (US) are
useful for pre-procedural planning to evaluate and manage
targeted biliary ducts for stent replacement before endo-
scopic re-intervention, and endoscopic procedures can be
carried out in a short time.

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Digestive Endoscopy 2017; 29: (Suppl. 2): 88–93 Management of occluded biliary stent 89

Management of cholangitis and the SEMS are the two main
considerations in these cases. Cholangitis is managed
according to guidelines, but the patient’s condition,
performance status, chemotherapy, myelosuppression, cancer
stage, and expected prognosis should also be considered.
Endoscopic biliary drainage is mandatory depending on the
timing, stent type, and procedure. Strategies to exchange a
SEMS or place a new stent through the initial one are not well
defined.
In addition, if acute cholecystitis occurs after SEMS
placement, it is sometimes difficult to diagnose which
biliary infection occurred: cholangitis with or without
cholecystitis, or cholecystitis without cholangitis. We should
take blood tests and dynamic CT to distinguish the status.
DISTAL BILIARY OBSTRUCTION
elucidated, and these two types of SEMS have similar
complication rates. Many endoscopists choose a covered
SEMS for an MBO because of similar efficacy and the
benefit of removability.
CASE PRESENTATION
A N 81-YEAR-OLD male patient had distal biliary
tract cancer and was at tumor stage IB (T2, N0, M0
UICC). Initially, we placed a PS before surgical treatment
(Fig. 1). However, acute cholangitis as a result of PS
occlusion occurred 2 weeks later, so the PS was exchanged
for endoscopic nasobiliary drainage (ENBD) (Fig. 2). We
exchanged the ENBD for a covered SEMS 4 days later
because of the patient’s wish for the best supportive care
(Fig. 3). He was admitted 5 months after placement of the
fully covered SEMS because of recurrent grade II cholan-

A DISTAL SIDE biliary obstruction is caused by

different types of malignant tumor, including pancre-
atic cancer, biliary tract cancer, gallbladder cancer, and
gitis according to Tokyo Guidelines 13. Clogging was
diagnosed by endoscopic retrograde cholangiopancreatog-
raphy (ERCP), and we cleared the clog with a balloon
lymph node metastasis. Endoscopic biliary drainage has catheter. No re-occlusion was detected after 7 months
been widely accepted as a palliative procedure for patients (Fig. 4).
with an unresectable distal malignant biliary obstruction
(MBO). Some studies have shown the superiority of SEMS
DISTAL BILIARY OBSTRUCTION CASES
compared with that of plastic stents (PS). Both covered and
uncovered SEMS are used for distal MBO cases, but these
two types of SEMS remain controversial. However, the
superiority of uncovered SEMS for patency has not been
W E CLEARED THE clog with a balloon to re-canalize
the initial covered SEMS and manage the cholangi-
tis. We used this approach because this case was not severe

(a)

(b)

Figure 1 Cholangiogram and placement of a plastic stent for distal biliary tract cancer. (a) Distal biliary stricture (white arrows).
(b) Placement of plastic stent (7 Fr Flexima stent; Boson Scientific Corp., Waltham, MA, USA). Bile juice flowing from the stent.

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90 H. Shiomi et al. Digestive Endoscopy 2017; 29: (Suppl. 2): 88–93

and the patient’s condition was good. Placing an ENBD tube

was another option, as these tubes can be used to check
drainage status, bile juice volume, and the causative bacteria
by culture. In addition, the tube can be washed if it becomes
occluded. Indication for placing an ENBD tube has not been
established, but we recommend this procedure in patients
with severe acute cholangitis. No subsequent procedure was
carried out in this case, and the covered SEMS was patent
with no complications until the patient died. Replacing a
covered SEMS after it becomes occluded with sludge has
been recommended by some authors; however, the initial
stent can be left in place to be cost-effective and reduce the
number of procedures.1,2 Another approach would be to
place a PS inside the initial covered SEMS. No controlled
comparative study has included this approach, and strong
evidence is needed to manage this condition using this
strategy. The utility of replacing a SEMS may be identified
in the future when the prognosis of patients with pancre-
atobiliary tract cancer is improved by further advances in
chemotherapy.2,3
An uncovered SEMS is another viable option to treat
distal MBO. Tumor ingrowth is the most common reason for
occlusion of an uncovered SEMS, and cleaning is not
Figure 2 Endoscopic nasobiliary drainage tube
appropriate in this situation. A PS or placing an ENBD tube
(pig-tail type) was re-placed to the occluded plastic
can be used to manage cholangitis, and an additional stent
stent.

(a)

(b)

Figure 3 Placement of a fully covered self-expandable metallic stent. (a) X-ray image after endoscopic placement across the
papilla. (b) Endoscopic view.

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Digestive Endoscopy 2017; 29: (Suppl. 2): 88–93
(a) (b)
Figure 4 Removal of sludge with a balloon catheter. (a) Cholangiogram showed occluded stent (white arrows). (b) Cleaning a
stent with a balloon catheter. (c) Endoscopic view of sludge coming out of a stent. (d) Balloon catheter. (e) After cleaning a
covered self-expandable metallic stent.
should be placed inside the initial uncovered SEMS.
Togawa et al. reported a retrospective comparative study
of occluded uncovered SEMS and inserted covered SEMS
in a stent-in-stent method, resulting in longer patency than
that of an uncovered SEMS and PS.4 No prospective data
have established the management procedure for an occluded
SEMS in cases of distal MBO.
HILAR BILIARY OBSTRUCTION
S EVERAL STUDIES HAVE shown that technical
placement success rates for PS and SEMS in patients
with distal MBO are similar, but the occlusion rate of a PS is
higher than that of a SEMS.5,6 Managing hilar MBO is
technically more complex than that of distal MBO because
of variations in hilar bile ducts. Mukai et al. reported a
prospective randomized controlled trial in which SEMS
were associated with longer stent patency, fewer complica-
tions, and better cost-effectiveness than those of a PS in
patients with hilar MBO. The authors suggested that SEMS
are more advantageous than PS for hilar and distal MBO.7
Recent advances in chemoradiotherapy for unresectable
pancreatobiliary malignancies have contributed to prolonged
survival. SEMS dysfunction occurs in 20–27% of patients8
and an occluded SEMS is associated with the development
Digestive Endoscopy © 2017 Japan Gastroenterological Endoscopy Society
Management of occluded biliary stent 91
(c)
(d)
(e)
of acute cholangitis. High-risk patients with cancer and the
elderly have an often-fatal complication of acute cholangitis,
which requires emergency drainage. However, no evidence
supports re-intervention for an occluded SEMS in patients
with unresectable hilar MBO. The number of stents,
choosing the drainage area, and the stenting configuration
(side-by-side or stent-in-stent) are somewhat controversial in
cases of hilar stenting with a SEMS. The re-intervention
procedure is influenced by these factors, and this informa-
tion should be considered before a re-intervention.
CASE PRESENTATION
T HE INITIAL SEMS was placed using the stent-in-stent
technique. After selective biliary duct cannulation, a
guidewire was inserted into the target biliary duct through
the SEMS and a small volume of contrast medium was
injected (Fig. 5a). Two guidewires were inserted into the
bilateral biliary duct (Fig. 5b), and an ENBD tube was
placed through the occluded SEMS along the guidewires
(Fig. 5c,d). If the stent would not pass through the SEMS
mesh, the mesh was dilated using a dilator and a balloon
catheter. After the cholangitis improved, the occluded SEMS
and the extent of the stricture were evaluated with contrast
medium injected into the ENBD tube (Fig. 6a). A wire-
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92 H. Shiomi et al. Digestive Endoscopy 2017; 29: (Suppl. 2): 88–93

(a) (b) (c) (d)

Figure 5 Emergency endoscopic drainage for acute cholangitis caused by occluded self-expandable metallic stent (SEMS) using
the stent-in-stent technique. (a,b) Two guidewires were advanced into each of the two targeted intrahepatic bile ducts through
the occluded SEMS. (c) Two nasobiliary drainage tubes were simultaneously advanced into the targeted intrahepatic bile ducts
through the occluded SEMS. (d) After withdrawing the endoscope.

(a) (b) (c)

2
2

Figure 6 Replacement of nasobiliary drainage (NBD) tube with a plastic stent (PS) in a stent-in-stent fashion. (a) Self-expandable
metallic stent (SEMS) occluded by tumor ingrowth or sludge (white arrows) was evaluated with contrast medium injected from
the NBD tube. (b) Sludge was cleaned from the SEMS using a wire-guided retrieval balloon catheter. Tumor ingrowth was
confirmed by intraductal ultrasonography. (c) A PS was advanced and placed along each guidewire in targeted intrahepatic bile
ducts through the occluded SEMS.

guided retrieval balloon catheter was used to clear debris, an
inflated balloon was pulled through the biliary duct, and
tumor ingrowth was confirmed by intraductal ultrasonogra-
phy (Fig. 6b). A PS was inserted through the occluded
SEMS for the tumor ingrowth (Fig. 6c).
HILAR OBSTRUCTION
However, no evidence supports endoscopic management
strategies for acute cholangitis caused by occlusion of a hilar
SEMS. If an occluded SEMS is suspected based on
symptoms and blood test results, emergency ERCP should
be carried out. An occluded SEMS increases intraductal
pressure, which eventually leads to cholangiovenous and
cholangiolymphatic reflux. Translocation of bacteria into the
bloodstream causes septicemia, which is often a fatal

T WO APPROACHES HAVE been used for endoscopic

or percutaneous transhepatic biliary drainage (PTBD)
when the initial SEMS is occluded in a hilar MBO. The
endoscopic biliary drainage is usually preferred as the first
choice because it is less invasive and preserves patient
quality of life. However, PTBD should be considered an
alternative approach if the endoscopic approach fails.
complication.
Patients with cholangitis have infected bile juice and sludge
in the biliary duct. If a large volume of contrast medium is
pushed into the biliary duct, bacteremia is induced by
cholangiovenous reflux. The targeting of bile duct which
should be drained was required in hilar MBO and determined
by MDCT or MRCP before ERCP. Three-phase (arterial,

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Digestive Endoscopy 2017; 29: (Suppl. 2): 88–93
portal, and equilibrium) contrast-enhanced CT is required in
hilar MBO cases and the arterial phase suggests the areas of
inflammation.9
A PS or an ENBD tube are placed for emergent biliary
drainage. The advantage of ENBD is that it allows the
monitoring of infected bile juice, washing out of debris by
saline injection, and measurements of tumor ingrowth after a
contrast medium injection. In contrast, the disadvantage is that
it causes stress to patients and confers the risk of self-removal
of the tube. After cholangitis improves, another stent should
be inserted to prevent the biliary obstruction due to tumor
ingrowth. A PS is generally used more commonly as the
second stent. Placing a PS is simple, has a high success rate,
and is easy to carry out as a re-intervention. A recent
systematic review of 10 retrospective studies revealed that
placing a PS may be as effective as placing a second SEMS.10
In contrast, Inoue et al. reported that the median time to a
recurrent biliary obstruction of a revisionary stent is signif-
icantly longer for placing a SEMS than that for placing a PS.11
The Tokyo Criteria use the term ‘recurrent biliary obstruction’
rather ‘patency’.12
CONCLUSION
I N CONCLUSION, We described management strategies
for acute cholangitis caused by occlusion of both distal and
hilar SEMS. Management of cholangitis and consideration of
drainage strategies differ between distal and hilar cases. Many
problems emerge regarding the drainage area, placement
method, and optimal stent type for the appropriate approach to
endoscopic palliation. Furthermore, re-intervention strategies
for occluded SEMS should be individualized, considering
patient condition or initial drainage, until more acceptable
results are found in randomized controlled trials that further
evaluate these issues.
CONFLICTS OF INTEREST
A UTHORS DECLARE NO conflicts of interest for this
article.
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