Introduction
Afferent limb syndrome (ALS), which shows chronic obstruction of the afferent limb
from various causes, is a postoperative complication following gastrointestinal surgery
[1]
[2]. Afferent limb obstruction can be caused by afferent limb kinking and angulation,
internal herniation, postoperative adhesions, or tumor recurrence. ALS may cause increased
epigastric pain, cholestasis, cholangitis, or pancreatitis. Previously, surgical treatment
was the definitive therapy for ALS [1]. However, in patients with malignant ALS due to recurrent cancer, less invasive
nonsurgical treatment is desirable considering the poor medical condition of the patients.
Recently, advances in endoscopic devices and techniques have led to various management
options [2]
[3]. Among them, treatment using a balloon enteroscope is also promising in complicated
reconstructive intestinal tract cases. However, there are apparently only a few case
reports of the treatment of malignant ALS by enteral self-expandable metal stent (SEMS)
placement using a balloon enteroscope [4]
[5]
[6]
[7]
[8]
[9], and little is known about the efficacy, safety, and follow-up results. We report
on enteral SEMS placement for malignant ALS using a single-balloon enteroscope (SBE)
in five consecutive patients and review previous case reports.
Case series
Between January 2010 and October 2017, we performed therapeutic endoscopic intervention
in five consecutive patients with malignant ALS using SBE. Informed consent to undergo
the procedure was obtained from each patient. We examined the procedural details and
clinical courses of the patients retrospectively using their medical records and endoscopic
database. This study was approved by our institutional review board.
Endoscopic procedures were performed using two types of SBE depending on the period:
standard SBE (SIF-Q260; Olympus, Tokyo, Japan) and short SBE (SIF-H290S; Olympus)
with an overtube. A standard SBE has a 200 cm working length and a 2.8 mm working
channel. A short SBE has a 152 cm working length and a 3.2 mm working channel. The
larger working channel of a short SBE has the advantage of allowing the use of up
to 9-Fr devices.
In all patients, the SBE was inserted into the afferent limb using a standard insertion
technique. After reaching the stricture site, enterography was performed and the stricture
length was confirmed. Then, a guidewire (0.025 inch VisiGlide2; Olympus, or 0.035
inch Jagwire; Boston Scientific, Tokyo, Japan) was inserted across the stricture.
In cases wherein it was difficult to recognize the accurate stricture site or length,
clip placement was performed as a landmark. Following guidewire placement, we performed
two types of procedure depending on the situation: the overtube-assisted (OA) method
or the through-the-scope (TTS) method. In the OA method, after the guidewire had been
placed deeply in the afferent limb across the stricture, the enteroscope was removed,
leaving the overtube fixed by the balloon and the guidewire in place. Subsequently,
an enteral SEMS (22 mm diameter, 60 – 120 mm long, Niti-S pyloric/duodenal D-type
stent; Taewoong Medical, Seoul, South Korea, or 22 mm diameter, 60 – 120 mm long,
WallFlex Duodenal stent; Boston Scientific) delivery system was advanced along the
guidewire through the remaining overtube. Thereafter, stent deployment was performed
under fluoroscopic guidance ([Fig. 1], [Video 1]). After the development of a newly designed enteral stent using a 9-Fr delivery
system (18 mm diameter, 60 – 120 mm long, Niti-S pyloric/Duodenal D-type stent; Taewoong
Medical or 22 mm diameter, 60 – 120 mm long, Wallflex Duodenal Soft stent; Boston
Scientific), we selected the TTS method using a short SBE. In the TTS method, after
the guidewire had been placed deeply across the stricture, an enteral SEMS was deployed
using direct endoscopic vision under fluoroscopic guidance ([Fig. 2], [Video 2]).
Fig. 1 Overtube-assisted SEMS placement. a Computed tomography (CT) showing marked dilation of the afferent limb (arrows) and
the recurrent tumor (arrowhead). b Endoscopic image of the stenotic site. c Enterography showing the afferent limb stenosis. The length of the stenosis was about
3 cm. d A marking clip was placed as a landmark for the stenotic site. e, f The enteral SEMS was deployed via the overtube.
Video 1 Overtube-assisted SEMS placement. After the guidewire had been placed across the
stricture, the enteroscope was removed, leaving the overtube and the guidewire in
place. Subsequently, SEMS deployment was performed under fluoroscopic guidance.
Fig. 2 Through-the-scope SEMS placement: a Fluoroscopic imaging showing malignant afferent limb obstruction. b The stent delivery system was introduced through the scope channel. c SEMS was deployed under direct endoscopic view with fluoroscopic guidance.
Video 2 Through-the-scope SEMS placement. After the guidewire had been placed across the
stricture, SEMS deployment was performed using direct endoscopic vision under fluoroscopic
guidance.
The main outcome measures were technical success and clinical success. Technical success
was defined as successful intended SEMS placement in the stricture site using an SBE.
Clinical success was defined as resolution of clinical symptoms and decreased dilation
of the afferent loop from the imaging findings. Adverse events (AEs) were evaluated
according to the severity grading system in the American Society for Gastrointestinal
Endoscopy’s lexicon.
After stent placement, each patient underwent physical examination daily and blood
test once a week until discharge. After discharge, each patient underwent physical
examination and blood test monthly in an outpatient clinic. The patients were advised
to visit the hospital if symptoms developed and they underwent further examination
including an imaging diagnostic test. If follow-up could not be carried out at our
institute, a telephone interview was conducted.
The clinical characteristics of the patients are summarized in [Table 1]. The primary diseases included pancreatic cancer (n = 4) and cholangiocarcinoma
(n = 1). The surgical methods for primary disease treatment included subtotal stomach
preserving pancreaticoduodenectomy in four patients (one received prior total gastrectomy)
and right hepatectomy with extrahepatic bile duct resection in one patient. The median
duration from surgery to endoscopic treatment was 21 months (range, 5 – 43 months).
All five patients had cholangitis, and their computed tomography (CT) images showed
afferent bowel loop dilatation due to recurrent tumor. The technical success rate
of the endoscopic treatment was 100 % in this case series. The median scope insertion
and total procedural times were 33 minutes (6 – 48 minutes) and 63 minutes (29 – 80
minutes), respectively. In four patients, SEMS was deployed using the OA method. In
the remaining case, SEMS was deployed using the TTS method. In all patients, the proper
position and expansion of the SEMS were confirmed on the following day by abdominal
radiography, and there were no post-procedural AEs. Clinical success was achieved
in all five patients postoperatively. Four patients died 219, 109, 103, and 84 days
after the procedure without recurrent cholangitis. The remaining patient had recurrent
cholangitis 114 days after the procedure, and CT showed bile duct dilation without
afferent limb obstruction. SBE-assisted endoscopic retrograde cholangiography through
the previously placed enteral SEMS revealed a choledochojejunal anastomosis stricture,
and balloon dilation of the anastomosis was performed. After the treatment, recurrent
cholangitis was not observed during the 651 days until the patient’s death. The details
of the endoscopic treatment procedure and the outcomes for each patient are summarized
in [Table 2].
Table 1
Characteristics of patients in our case series.
|
Patient
|
Age (years), sex
|
Primary disease
|
Reconstruction method
|
Duration after surgery (months)
|
Indication
|
Cause of ALS
|
|
1
|
76 M
|
Pancreatic cancer
|
SSPPD (earlier total gastrectomy with Roux-en Y reconstruction)
|
42
|
Cholangitis
|
Recurrent tumor
|
|
2
|
65 M
|
Pancreatic cancer
|
SSPPD
|
5
|
Cholangitis
|
Recurrent tumor
|
|
3
|
59 F
|
Pancreatic cancer
|
SSPPD
|
21
|
Cholangitis
|
Recurrent tumor
|
|
4
|
77 M
|
Pancreatic cancer
|
SSPPD
|
7
|
Cholangitis
|
Recurrent tumor
|
|
5
|
64 M
|
Cholangiocarcinoma
|
Right hepatectomy with bile duct resection
|
43
|
Cholangitis
|
Recurrent tumor
|
ALS, afferent limb syndrome; SSPPD, subtotal stomach preserving pancreaticoduodenectomy.
Table 2
Details of endoscopic treatment in our case series.
|
Patient
|
Scope
|
Stent deployment method
|
Stent
|
Procedure time (min)
|
Adverse events
|
Follow-up period (days)
|
Recurrent cholangitis
|
|
Delivery system size (Fr)
|
Diameter (mm)
|
Length (mm)
|
|
1
|
Short SBE
|
Overtube assisted
|
10
|
22
|
120
|
80
|
None
|
219
|
No
|
|
2
|
Short SBE
|
Overtube assisted
|
10
|
22
|
80
|
68
|
None
|
103
|
No
|
|
3
|
Short SBE
|
Overtube assisted
|
10
|
22
|
100
|
29
|
None
|
109
|
No
|
|
4
|
Short SBE
|
Through-the-scope
|
9
|
22
|
60
|
56
|
None
|
84
|
No
|
|
5
|
Standard SBE
|
Overtube assisted
|
10
|
22
|
60
|
63
|
None
|
765
|
Yes (choledochojejunal anastomosis stenosis 114 days after the procedure)
|
SBE, single-balloon enteroscope.
Discussion
We confirmed the efficacy and safety of enteral SEMS placement using SBE in five patients
with malignant ALS. ALS is a postoperative complication in various gastrointestinal
surgeries [1]
[2]. The incidence of ALS in pancreatic cancer patients after pancreaticoduodenectomy
is reported to be 13 % [2]. In addition, one-third of the ALS in this population was caused by recurrent pancreatic
cancer.
Although surgery is the standard therapy for ALS, it is highly invasive for patients
with noncurative malignant disease, particularly pancreatobiliary cancer. On the other
hand, the percutaneous transhepatic approach is a well-established treatment for ALS
[10]. However, it usually requires two steps: percutaneous transhepatic biliary drainage
(PTBD) and stent placement along the PTBD tract 1 or more weeks later. Therefore,
the percutaneous approach is relatively invasive and time-consuming. Although the
one-step direct percutaneous enteral stent insertion technique has also been reported,
it has a high risk of bile leakage. Furthermore, in patients without intrahepatic
bile duct dilation, the percutaneous approach is difficult and occasionally not possible.
On the other hand, enteroscopy enables patients to undergo one-step enteral metal
stent placement which can contribute to the maintenance of a patient’s quality of
life [2]
[3]. In addition, enteroscopy can be performed in patients with a bleeding tendency
(e. g., severe coagulopathy or receiving anticoagulation therapy) who are at a high
risk for surgery and percutaneous treatment. However, in patients with a long and
tortuous afferent bowel loop before stenosis, the endoscopic approach is thought to
be difficult.
At present, balloon enteroscope-assisted endoscopic intervention includes enteral
metal stent placement, which is applied in the treatment of several conditions in
patients with surgically altered anatomy. In our PubMed search, there were six reports
(eight patients) in which SEMS was placed for the treatment of malignant ALS using
a balloon enteroscope ([Table 3]) [4]
[5]
[6]
[7]
[8]
[9]. Four patients were treated using the OA method and the remaining four patients
using the TTS method. SEMS placement on the target site was successful in all patients;
subsequently, clinical success was achieved. Recently, a newly designed balloon enteroscope
with a shorter scope length and a larger working channel, and enteral SEMS with a
smaller delivery system enabled us to perform TTS SEMS placement under direct endoscopic
view with fluoroscopic guidance. This technique appears to be easier, safer, and more
accurate than OA SEMS placement [7]
[8]
[9].
Table 3
Summary of other studies using enteral metal stent placement for malignant afferent
limb syndrome with a balloon enteroscope.
|
Reference
|
Number of patients
|
Primary disease
|
Reconstruction method
|
Scope
|
Stent deployment method
|
Stent
|
Clinical success
|
Adverse events
|
Outcome
|
|
Diameter (mm)
|
Length (mm)
|
|
Kida et al. 2013 [4]
|
1
|
Pancreatic cancer
|
PPPD
|
Standard DBE
|
Overtube assisted
|
NA
|
NA
|
Yes
|
None
|
NA
|
|
Sasaki et al. 2014 [5]
|
1
|
Pancreatic neuroendocrine carcinoma
|
PD with R-Y
|
Standard DBE
|
Overtube assisted
|
22
|
60
|
Yes
|
None
|
NA
|
|
Nakahara et al. 2015 [6]
|
2
|
Pancreatic cancer (1), cholangiocarcinoma (1)
|
PPPD (2)
|
Standard SBE
|
Overtube assisted
|
22
|
120
|
Yes
|
Ascending cholangitis (1)
|
No recurrent cholangitis (4 months, 14 months)
|
|
Shimatani et al. 2016 [7]
|
1
|
Pancreatic cancer
|
PD
|
Short DBE
|
Through-the-scope
|
18
|
60
|
Yes
|
None
|
NA
|
|
Minaga et al. 2016 [8]
|
1
|
Duodenal cancer
|
PD
|
Short SBE
|
Through-the-scope
|
18
|
80
|
Yes
|
None
|
NA
|
|
Kanno et al. 2018 [9]
|
2
|
Cholangiocarcinoma (1), gastric cancer (1)
|
PD (1), TG with R-Y
|
Short SBE
|
Through-the-scope
|
18
|
80, 100
|
Yes
|
None
|
No recurrent cholangitis (1 month, 12 months)
|
PD, pancreaticoduodenectomy; PPPD, pylorus-preserving pancreaticoduodenectomy; DBE,
double-balloon enteroscope; R-Y, Roux-en Y reconstruction; SBE, single-balloon enteroscope;
TG, total gastrectomy.
To the best of our knowledge, there have been few reports to date about post-procedural
outcomes after endoscopic enteral SEMS placement for malignant ALS [6]
[9]. Our case series showed satisfactory follow-up results without apparent recurrent
cholangitis due to obstruction of the enteral SEMS over the remaining life of the
patients. Furthermore, it is theoretically possible to perform additional SEMS placement
if SEMS occlusion occurs.
Enteral SEMS placement using SBE is an effective, less invasive, promising treatment
method for malignant ALS. Further accumulation of cases, examination of safety and
efficacy, and evaluation of follow-up results are warranted to confirm our results.