ORIGINAL ARTICLE: Clinical Endoscopy

The risk of post-ERCP pancreatitis and the protective effect of rectal

indomethacin in cases of attempted but unsuccessful prophylactic
pancreatic stent placement
Neel S. Choksi, MD,1 Evan L. Fogel, MD, MSc,2 Gregory A. Cote, MD, MS,2 Joseph Romagnuolo, MD, MS,3
Grace H. Elta, MD,1 James M. Scheiman, MD,1 Amitabh Chak, MD,4 Patrick Mosler, MD, PhD,5,6
Peter D. R. Higgins, MD, PhD, MSc,1 Sheryl J. Korsnes, MA,1 Suzette E. Schmidt, BSN, CCRP,2
Stuart Sherman, MD,2 Glen A. Lehman, MD,2 B. Joseph Elmunzer, MD,1 on behalf of the
United States Cooperative for Outcomes Research in Endoscopy
Ann Arbor, Michigan, USA

Background: It is believed, based on limited observational data, that an unsuccessful attempt to place a prophylactic pancreatic stent substantially increases the risk of post-ERCP pancreatitis (PEP).
Objective: To better understand the risk of PEP in patients with failed pancreatic stent placement (FPS) and
the impact of rectal indomethacin on this risk.
Design: Secondary analysis of randomized, controlled trial data.
Setting: University of Michigan and Indiana University.
Patients: A total of 577 clinical trial participants at elevated risk for PEP.
Interventions: Pancreatic stent placement.
Main Outcome Measurements: Within the placebo group, we compared PEP rates in patients with FPS,
patients who underwent successful stent placement, and in those without a stent attempt. We also performed
a regression analysis evaluating the association between FPS and PEP. To dene the protective effect of indomethacin, we repeated these analyses in the indomethacin group and in the full study cohort.
Results: The incidence of PEP among patients in the placebo group who experienced FPS was 34.7%, signicantly exceeding rates in patients who underwent successful stent placement (16.4%) and in those without a stent
attempt (12.1%). After we adjusted for known PEP risk factors, FPS was found to be independently associated with
PEP. Among the indomethacin group and in the full cohort, FPS was not associated with a higher risk of PEP.
Limitations: Low event rate, FPS not prospectively captured.
Conclusion: FPS appears to confer an increased risk of PEP, which is attenuated by rectal indomethacin administration. These ndings highlight the importance of adequate training and prociency before endoscopists
attempt pancreatic stent placement and the routine use of rectal indomethacin in high-risk ERCP cases. (Gastrointest Endosc 2015;81:150-5.)
(footnotes appear on last page of article)

Prophylactic pancreatic stent placement (PSP) reduces

the risk of post-ERCP pancreatitis (PEP) by preventing
pancreatic ductal hypertension and the consequent

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activation of trypsin that develop as a result of

transient procedure-induced obstruction of the pancreatic orice. Randomized, controlled trial (RCT) data
demonstrate that PSP reduces the incidence of PEP by
approximately 70% and essentially eliminates the risk
of severe pancreatitis.1,2 As such, PSP is widely regarded
as an effective means of preventing PEP in high-risk
cases, is commonly used in the United States,3 and is
recommended by the European Society of Gastrointestinal Endoscopy.4

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Choksi et al

Although PSP clearly reduces risk, it is associated

with several important disadvantages. It can be technically
challenging, time consuming, costly, and inconvenient for
patients.5-8 Perhaps the most important clinical disadvantage of PSP is the belief that attempting to place a pancreatic stent with subsequent failure substantially increases
the risk of PEP by inducing additional injury to the pancreatic orice and/or pancreatic duct without providing
ductal decompression.9 Because data evaluating the success rates and effectiveness of PSP in real-world practice,
as opposed to expert centers, are not available, this phenomenon of attempted but failed pancreatic stent placement (FPS) may represent an underappreciated problem
in ERCP practice.
Our understanding of FPS and its implications is based
entirely on anecdotal evidence and a single observational
study comprising only 3 outcome events wherein a single
expert endoscopist placed all the pancreatic stents.9
Our group recently published a large-scale, multicenter
RCT showing that rectal indomethacin reduced the risk
of PEP in high-risk patients, most of whom (O80%) had
undergone PSP.10 A subset of participants in this RCT,
randomly assigned to receive rectal indomethacin or placebo, experienced FPS.
By using these multicenter RCT data, we aimed to
better understand the phenomenon of FPS by (1) determining the incidence of PEP in high-risk ERCP cases
complicated by FPS, (2) assessing the prophylactic effect
of indomethacin in patients with FPS, and (3) performing
an exploratory evaluation of clinical and procedural factors
associated with FPS.

Rectal indomethacin

This study was a secondary analysis of prospectively

collected data obtained during a previously reported multicenter RCT of rectal indomethacin for preventing PEP.10
Briey, after approval by the institutional review committees of the involved centers, patients at elevated risk for
PEP were randomly assigned to receive 100 mg of rectal
indomethacin or placebo suppositories immediately after
ERCP. All other procedural and clinical decisions were deferred to the treating physicians. Placement of a pancreatic
duct stent was not mandated; however, O80% of patients
received a stent because the study enrolled patients at
elevated risk for PEP. The primary endpoint of the study
was the development of PEP, dened as new onset of
pain in the upper abdomen, an elevation in pancreatic
enzyme levels of R3 times the upper limit of the normal
range 24 hours after the procedure, and hospitalization
for at least 2 nights.11 Patient demographics, risk factors
for PEP, ERCP procedure details, and follow-up data were
recorded on standardized data collection forms by a member of the study team who was blinded to study group
assignment. All data were subsequently entered into a

Web-based database and managed by an independent

data management service. The nal database contained
information on 602 study participants.
We included all RCT participants enrolled at 2 study
centers (Indiana University, University of Michigan),
comprising 96% of total enrollment. To generate a study
sample of FPS participants, we identied the subset of participants in the RCT who did not have a pancreatic stent
placed at the time of ERCP. Two investigators (N.C.,
B.J.E.) who were unaware of study group assignment and
outcome then independently reviewed the procedure reports for each of these participants to adjudicate whether
an attempt at PSP was made by using a prioridetermined
criteria. A patient was deemed to have experienced FPS
if 1 or more of the following criteria was explicitly present
in the procedure report: (1) PSP was unsuccessful despite
attempt; (2) pancreatic duct cannulation could not be
achieved despite attempt; (3) there was failed cannulation
of both the bile duct and pancreatic duct; (4) pancreatic
duct cannulation was achieved, but the wire was lost
before stent placement; and (5) pancreatic duct cannulation was achieved, but the ERCP was aborted before
completion of the procedure. In the context of a highrisk case, criteria 2 and 3 assumed that cannulation is the
rst and necessary element of successful PSP, and the
inability to achieve cannulation represents a failure of all
endoscopic objectives, including PSP. Criteria 4 and
5 assumed that, during a high-risk case, placement of a
wire into the pancreas indicates that PSP is already underway, and a prophylactic stent would have been placed had
access not been lost. In cases of pancreas divisum, the dorsal pancreatic duct was considered the duct of interest. Patients who did not have a pancreatic stent placed and did
not meet any of the 5 FPS criteria made up the no PSP
attempt cohort.
To estimate the risk of PEP associated with FPS independent of the effect of indomethacin, we restricted the primary analysis to participants in the placebo group of
the RCT. Within this group, we compared the risk of PEP
in patients with FPS, in patients who underwent successful
stent placement, and in patients who did not undergo an
attempt at PSP. In addition, we performed an exploratory
multivariable logistic regression analysis evaluating the
association between PEP (dependent variable) and FPS
(main predictor variable) while adjusting for PEP risk in
two separate ways: (1) by including patients PEP risk
scores as a covariate in one model and (2) by including
scores for patients propensities to receive a pancreatic
stent in another model. The PEP risk score, which has
been described previously, was calculated for each participant by assigning 1 point for each major RCT inclusion criterion and 0.5 point for each minor RCT inclusion criterion
(Table 1).10 The propensity score predicts a participants
conditional probability of receiving a pancreatic stent
based on all other observed characteristics of that participant, serving as a surrogate marker for PEP risk.

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METHODS

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Choksi et al

RESULTS
TABLE 1. Major and minor study inclusion criteria
used to calculate post-ERCP pancreatitis risk score
Major criteria

Minor criteria

Clinical suspicion of
sphincter of Oddi
dysfunction

Age !50 y and female

History of post-ERCP
pancreatitis

History of recurrent
pancreatitis

Pancreatic sphincterotomy

Precut (access)
sphincterotomy
O8 cannulation attempts

R3 pancreatic injections,
with at least 1 injection
to the tail
Pancreatic acinarization
Pancreatic brush cytology

Pneumatic dilation of
intact biliary sphincter
Ampullectomy

To assess the protective effect of indomethacin, these

analyses were then repeated in the group of participants
assigned to receive indomethacin and in the full RCT
cohort (placebo and indomethacin groups). To evaluate
the modifying effect of indomethacin on FPS, in the
regression analysis of the full cohort we included an interaction variable containing FPS and study group
assignment.
An exploratory analysis of clinical and procedural factors
associated with FPS was conducted by performing sequential univariate logistic regression analyses, with FPS as the
dependent variable and the following predictor variables:
age, sex, study center, suspicion of sphincter of Oddi
dysfunction, prior PEP, recurrent pancreatitis, pancreatic
sphincterotomy, precut sphincterotomy, difcult cannulation, ampullectomy, pancreatic brush cytology, manometrically proven sphincter dysfunction, biliary sphincterotomy,
bile duct stent placement, choledocholithiasis, pancreaticobiliary malignancy, trainee involvement, and pancreatic
acinarization. Any variable positively associated with FPS
(P value ! .05) in the univariate analysis was included
in a multivariable logistic regression model with FPS as
the dependent variable. Seven predictor variables were
included in the nal model: age, sex, study site, recurrent
pancreatitis, difcult cannulation, choledocholithiasis, and
trainee involvement.
All statistical analyses were performed by using the
STATA 12 statistical package (StataCorp LP, College Station, Tex). The difference in the proportion of PEP between groups was analyzed by using the Fisher exact
test, with a 2-tailed P value of ! .05 indicating signicance.
Propensity score calculation was conducted by using the
psmatch2 command.
152 GASTROINTESTINAL ENDOSCOPY Volume 81, No. 1 : 2015

A total of 577 RCT participants were included in this

analysis. Forty-two participants experienced FPS (7.3%),
which occurred in 10 of the 403 participants enrolled at
Indiana University (2.4%) and 32 of the 164 participants
enrolled at the University of Michigan (19.5%). Seventyseven of the 577 participants experienced PEP (13.3%);
the PEP rate was 17.3% (51 of 294) in the placebo group
and 9.2% (26 of 283) in the indomethacin group.

The risk of PEP associated with FPS in the

placebo group
A total of 294 RCT participants were randomized
to receive placebo. Of these, 23 (7.8%) experienced FPS.
Eight of the 23 FPS cases (34.7%) resulted in PEP
compared with 39 of the 238 successful PSP cases
(16.4%; P Z .04) and 4 of the 33 cases in which there
was no attempt at PSP (12.1%; P Z .02) (Fig. 1). Among
participants in the placebo group, a logistic regression
model adjusting for PEP risk showed that FPS was independently associated with PEP (odds ratio [OR] 3.24; 95% condence interval [CI], 1.26-8.31 adjusted by PEP risk score;
OR 3.15; 95% CI, 1.14-8.77 adjusted by pancreatic stent
propensity score).

The protective effect of rectal indomethacin in

patients with FPS
Of the 283 patients who received indomethacin,
19 (6.7%) experienced FPS. Only 1 (5.3%) of these 19 patients with FPS developed PEP, compared with 23 of the
239 patients who underwent successful stent placement
(9.6%; P Z 1.0) and 6 of the 58 patients who did not
undergo a PSP attempt (10.3%; P Z 1.0) (Fig. 1).
In a comparison of FPS within the entire cohort (indomethacin and placebo groups), 8 of the 23 patients with
FPS in the placebo group developed PEP (34.7%), whereas
only 1 of the 19 patients with FPS in the indomethacin
group developed PEP (5.3%) (P Z .027). Logistic regression analysis of the full RCT cohort demonstrated that
FPS is independently associated with PEP only when an
interaction variable making up the FPS and study group
assignment is included in the model, further supporting indomethacins protective effect on PEP in patients who
experienced FPS.

Factors associated with FPS

The exploratory risk factor analysis revealed that
increasing age (OR 1.03; 95% CI, 1.01-1.06), study site (University of Michigan) (OR 6.87; 95% CI, 3.03-15.59), a history
of recurrent pancreatitis (OR 2.19; 95% CI, 1.06-4.54),
and difcult cannulation (OR 3.79; 95% CI, 1.84-7.79) are
independently predictive of FPS.
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Choksi et al

Rectal indomethacin

Figure 1. Risk of PEP among patients with FPS compared with no attempt and successful PSP in the placebo group (left panel ) and indomethacin
group (right panel ). PEP, post-ERCP pancreatitis; PSP, pancreatic stent placement; FPS, failed pancreatic stent placement.

DISCUSSION
This secondary analysis of RCT data suggests that patients who experienced attempted but failed PSP were
at signicantly increased risk for PEP compared with patients who underwent successful stent placement and
those in whom stent placement was not attempted. Prophylactic administration of rectal indomethacin appears
to signicantly attenuate this risk. Exploratory risk factor
analysis suggests that a history of recurrent pancreatitis
and difcult cannulation are clinical factors associated
with FPS.
In this RCT, the PEP risk in patients who experienced
FPS but did not receive indomethacin was approximately
35%. Although this risk is not as high as previously reported
in a small, non-controlled series,9 it is certainly higher than
the rate of PEP observed among patients who underwent
successful stent placement in our RCT and in numerous
other RCTs evaluating the protective effect of PSP,
wherein the rate of PEP in patients who underwent successful stent placement ranged from 2% to 15%.6,7,12-15
The risk of PEP associated with FPS we observed
also appears to exceed the risk seen in the control arms
of previously published RCTs involving PSP, wherein stent
placement was not attempted and pancreatitis occurred in
13% to 29% of cases.6,7,12-15 In our RCT, the rate of PEP was
considerably (3-fold) higher in the FPS group than in the
no attempt group, although this observation is confounded
by the fact that the decision to place a pancreatic stent in
this RCT was deferred to the discretion of the endoscopist.
Patients in whom stent placement was not attempted were
likely to be at lower risk for PEP because they elicited less
concern on the part of the endoscopist.16 Nevertheless, a
logistic regression model adjusting for this confounding

also suggested that FPS is an independent predictor of

PEP.
PSP can be a challenging intervention that is not
always technically feasible. Indeed, prior studies have reported FPS rates in the 5% to 10% range.6,7,15 These
studies were performed at referral medical centers by endoscopists with expertise and experience in pancreatic
endoscopy. Although broader data from academic and
community practices are not available, FPS is likely to be
an underappreciated, and perhaps growing, problem in
real-world ERCP practice. In this context, the results of
this study underscore the importance of (1) adequate
training, experience, and procedure volume for those performing high-risk ERCP requiring PSP; (2) a responsible
approach to referring high-risk cases that mandate PSP
to tertiary-care centers; and (3) the routine use of rectal
indomethacin in all high-risk cases. Some experts recommend rectal indomethacin for all patients undergoing
ERCP based on highly favorable cost and risk benet
ratios as well as existing RCT data suggesting its efcacy
across the entire spectrum of PEP risk.17,18 However, given
the potential for FPS and its consequences, the ndings
of this study suggest that rectal nonsteroidal antiinammatory drug administration is particularly important
in high-risk cases, such as those that would have been
included in our RCT (Table 1).
A major question surrounding PSP is the acceptable
amount of time and effort that should be spent on the
insertion process in cases of difcult pancreatic access. Presumably, there exists a point of diminishing return at which
the risk of additional attempts outweighs the benet of
stent placement, especially if insertion eventually proves
unsuccessful. Because future clinical studies are unlikely
to answer this question in a methodologically rigorous

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Choksi et al

fashion, endoscopists should be aware of this important

clinical balance and use their best judgment regarding
acceptable stent placement efforts. Based on the results
of this study, it may be reasonable to favor a strategy of
limited PSP efforts (and rectal indomethacin) when pancreatic access proves challenging, especially in patients with
prior recurrent pancreatitis or when a difcult biliary cannulation has occurred.
In this RCT, we observed a signicant difference in FPS
rates between study sites. Because FPS was not dened a
priori, the approach to PSP was not standardized, and
data on several factors that are potentially important in
the success or failure of stent placement are not available,
the underlying causes of this difference cannot be dened
concretely. However, several potential explanations exist.
First, systematic differences between centers in dening
FPS or in the time and effort dedicated to PSP before the
decision to abort may have played a role. Additionally,
technical differences between centers, including the
choice of endoscopic instruments, may have been important. In particular, some experts advocate the routine use
of .018-inch guidewires for FPS to more safely and effectively negotiate potentially tortuous pancreatic ducts;
others advocate catheter systems that allow endoscopist
control of the guidewire. Additional research is necessary
to elucidate whether these or other factors are important
in minimizing the FPS rate and in attenuating the risk of
PEP when FPS occurs.
Despite the ndings of this study, PSP remains the standard of care for preventing PEP in high-risk patients, based
on robust clinical trial data and existing guidelines. However, considering the implications of FPS as well as the other
potential disadvantages of PSP, future research focused on
dening prophylactic strategies that allow more selective
PSP use would be of signicant clinical value. For example,
a previously published post hoc analysis of this RCT16 and a
network meta-analysis19 have suggested that rectal indomethacin mono-prevention could be equivalent to, if not
superior to, the combination of indomethacin and PSP
in high-risk cases. On this basis, a large-scale, multicenter
RCT comparing rectal indomethacin alone versus combination therapy is in the nal planning phases and should
begin enrolling participants in early 2015. Furthermore,
post-traumatic pancreatic orice edema and stenosis
may be mitigated by other pharmacologic agents such
as nitroglycerin20 and topically applied epinephrine.21
Additional studies are necessary to determine whether
these agents can serve as a surrogate stent, providing
ductal decompression without the risks, costs, and inconvenience of PSP.
The results of this study should be considered in the
context of 2 important limitations. First, our RCT data
collection form did not prospectively capture FPS. This
endpoint was adjudicated post hoc by manual review of
procedure reports by using the aforementioned criteria
that are based on clinical assumptions aiming to determine

endoscopist intent. Although we believe these assumptions are reasonable, FPS may have been under-captured
(when stent attempt was not mentioned) or misclassied
(if the description of the procedure was misinterpreted
by the reviewer), potentially biasing study results. Second,
the event rate in this study was small, reducing the precision in our estimates of effect and leading to probable
regression model overtting and possible missed associations because of low statistical power. Nevertheless, this
is the largest and most methodologically rigorous analysis
of the phenomenon of FPS, and it provides important, clinically relevant data in this area. To shed additional light on
PSP and the phenomenon of FPS, researchers in future
RCTs involving ERCP should prospectively collect data on
the endoscopic instruments (catheters, wires, and stents)
used for PSP; underlying pancreatic duct anatomy; the
duration, technical difculty, effort, and personnel involved
in the attempt; and the reasons for failure.
In summary, attempted but failed pancreatic stent placement appears to confer an increased risk of PEP, which
is attenuated by prophylactic rectal indomethacin administration. These ndings highlight the importance of
adequate training and prociency for the endoscopist
before PSP is attempted and routine use of rectal indomethacin in high-risk ERCP cases. Given the risks and costs
of PSP, identifying prophylactic strategies that minimize
the need for pancreatic stenting may be of substantial clinical and economic value.

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Volume 81, No. 1 : 2015 GASTROINTESTINAL ENDOSCOPY 155

Abbreviations: FPS, failed pancreatic stent placement; PEP, post-ERCP

pancreatitis; PSP, pancreatic stent placement; RCT, randomized,
controlled trial.
DISCLOSURE: All authors disclosed no financial relationships relevant
to this article.
See CME section; p. 214.
Copyright 2015 by the American Society for Gastrointestinal Endoscopy
0016-5107/$36.00
http://dx.doi.org/10.1016/j.gie.2014.07.033
Received April 3, 2014. Accepted July 11, 2014.
Current affiliations: Division of Gastroenterology, University of Michigan
Medical Center, Ann Arbor, Michigan (1), Division of Gastroenterology,
Indiana University Medical Center, Indianapolis, Indiana (2), Division of
Gastroenterology, Medical University of South Carolina, Charleston,
South Carolina (3), Division of Gastroenterology, University Hospitals
Case Medical Center, Cleveland, Ohio (4), Division of Digestive Diseases
and Nutrition, University of Kentucky Medical Center, Lexington,
Kentucky, USA (5), Division of Gastroenterology and Hepatology,
Kantonsspital Graubuenden, Chur, Switzerland (6).
Reprint requests: Neel Choksi, MD, University of Michigan Medical Center,
3912 Taubman Center, Ann Arbor, MI 48109.