6/11/2014 Uses of endoscopic retrograde cholangiopancreatography in the management of post-cholecystectomy complications

Uses of endoscopic retrograde cholangiopancreatography in the management

of post-cholecystectomy complications

Seerwan HS Qaradaghy1 (quaradaghi at gmail dot com) #, Taha A Alkarboly2 , Ali A Ramadhan3 , Habeeb M Abdullah4 , Tahir AH
Hawramy1
1 Department of General Surgery, School of Medicine, Faculty of Medical Sciences, University of Sulaimani; Department of General

Surgery, Sulaimani Teaching Hospital, Sulaimani, Kurdistan Region-Iraq. 2 Department of Medicine, School of Medicine, Faculty of
Medical Sciences, University of Sulaimani; Kurdistan Center for Gastroenterology and Hepatology, Sulaimani, Kurdistan Region-Iraq. 3
Kurdistan Center for Gastroenterology and Hepatology, Sulaimani, Kurdistan Region-Iraq; Department of Medicine, School of Medicine,
Faculty of Medical Sciences, University of Duhok, Duhok, Kurdistan region-Iraq. 4 Department of General Surgery, Sulaimani Teaching
Hospital, Sulaimani, Kurdistan Region-Iraq

# : corresponding author

DOI http://dx.doi.org/10.13070/rs.en.1.770
Date 2014-05-09
Cite as Research 2014;1:770
License CC-BY

Abstract
Background: Post-cholecystectomy complications represent a significant clinical problem.
Endoscopic Retrograde Cholangiopancreatography (ERCP) has largely replaced surgery to manage these
complications by having a diagnostic as well as a therapeutic role. Objective: To document the extent of post-
cholecystectomy biliary complications and evaluate the role of ERCP in their management. Patients and
method: Over a period of one year, 55 patients were received with history of cholecystectomy within 2 years
prior to presentation. Those with non-biliary related complications were excluded. All patients underwent ERCP
with therapeutic interventions guided by the diagnosis obtained from the initial cholangiogram. They were
followed up for 3 months to determine the outcome. Results: The age range was 20 to 80 years with a mean of
42 years. The female to male ratio was 5:1. Thirty eight patients were operated upon laparoscopically and 17
patients by open method. The most frequent presentation was abdominal pain (N = 27, 49.1%). The most
common finding during ERCP was retained bile duct stones (N=32, 58.2%) followed by bile duct injuries (N=19,
34.5%). The overall success rate for endoscopic intervention was 83.6% (N=46). The most common
complication of ERCP was pancreatitis (N=3, 5.5%). Three patients died (5.5%). There was no significant
statistical association between the type of cholecystectomy and findings on ERCP, success of ERCP
intervention or complications of ERCP (P > 0.05). Conclusion: The commonest post-cholecystectomy
complications were retained bile duct stones followed by bile duct injuries. ERCP is an effective and safe method
in the diagnosis and management of these complications.

Introduction
Nowadays laparoscopic cholecystectomy is the treatment of choice for symptomatic gallstones [1]. Despite its
advantages in decreasing postoperative pain and length of stay with faster recovery [2], it carries a two folds higher
rate of complications than open method (0.6% versus 0.3%) [3], regardless of all the developments in the
knowledge, technology and techniques [2].

These complications markedly affect the patient’s quality of life over long follow up periods [4]. They can be biliary
related in the form of retained bile duct substance (stones or parasites) and bile duct injury or non-biliary related
like visceral and vascular injuries [5]. About 30% of these complications are recognized intra-operatively with the
rest presenting at variable intervals later on [6].

Endoscopic Retrograde Cholangiopancreatography (ERCP) has largely replaced surgery in the management of
these problems [3] as it has comparable success rates and lower morbidity and mortality [7]. It has a definitive role
in establishing diagnosis, defining the site and severity of injury in addition to providing therapeutic interventions
[4]. The aim of this study is to document the extent of post-cholecystectomy biliary complications in our region with
evaluation of the ERCP role in their management.

Patients and Method

This prospective study was conducted at Kurdistan Center for Gastroenterology and Hepatology (KCGH), a tertiary
referral center in Sulaimani governorate – Iraq, over a period of one year (from January, 2012 to January, 2013).

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We received 55 patients who had cholecystectomies within 2 years [8] and were referred on the assumption of
having complications related to their previous operation. Their complaints were abdominal pain (mainly right
hypochondrial pain), jaundice, fever, abdominal distension or leakage from the drain or the wound. Patients with
non-biliary related complications were excluded.

All patients were interviewed before the procedure to document the clinical data (details of previous surgery,
presenting symptoms and time interval between surgery and symptoms). The initial diagnostic work up included
liver biochemical tests and trans-abdominal ultrasound. Selected cases underwent computed tomography (CT)
scan, endoscopic ultrasound (EUS) and / or magnetic resonance cholangiopancreatography (MRCP) as dictated
by the clinical presentation and the results of the initial work up.

After taking the informed consent, ERCP was performed under conscious sedation with pulse oximetry monitoring
by an experienced gastroenterologist. A basic cholangiogram was obtained to determine the nature and site of the
abnormality and then therapeutic interventions were performed accordingly.

Bile duct injuries were classified according to Bergman’s classification which was used to guide our management
strategy. This includes four types of bile duct injuries. Type-A were peripheral leaks including those from the cystic
duct and treated with sphinecterotomy and/or stent insertion for 6 weeks. Type-B were major bile duct leaks and
managed with stenting for 3 months. Type-C were bile duct strictures treated with sequential stenting. Type-D were
bile duct transections that were referred for surgical operation [9].

After the ERCP, patients were kept under observation in KCGH for 4-6 hours. Those with suspected post-ERCP
complications or failed ERCP were admitted to the hospital for further management. After discharge, patients were
followed up in the outpatient clinic after one week and then once a month for 3 months. On each follow up visit,
they were questioned about their symptoms and investigations like liver biochemical tests and trans-abdominal
ultrasound were performed.

Analysis of data using Statistical Package for the Social Sciences (SPSS) program version 19.0 for windows was
done. Statistical analysis was conducted to calculate the P-value using χ2. For the associations to be significant,
the P-value should be less than 0.05 [10].

Results
The age range was 20 to 80 years with a
SN Parameters Number Percentage
mean of 42 years and 39 patients (71%) were
1 Clinical presentation less than 50 years old. Females were 46
1.1 Abdominal pain 27 49.1% (84%) and males were 9 (16%) with a female
1.2 Jaundice 15 27.3% to male ratio of 5:1. Cholecystectomy was
done laparoscopically in 38 patients (69%)
1.3 Drainage from drain or from skin 13 23.6%
and by open method in 17 patients (31%). The
2 Duration from surgery to presentation
most common presentation was abdominal
2.1 Less than 1 week 19 34.6% pain (N = 27, 49.1%). The time interval
2.2 1 week to 1 month 16 29.1% between surgery and presentation was less
2.3 1 month to 1 year 13 23.6% than 1 week in 19 patients (34.5%) while 7
2.4 More than 1 year 7 12.7%
patients (12.7%) presented after a year.
Table-1 shows the clinical data of the study
Table 1. Clinical data of study population (N = 55): About half of patients population.
presented with abdominal pain. The time interval between surgery and
presentation was less than 1 week in one third of patients.
The laboratory data are shown in table-2.

Parameter Aspartate Alanine Alkaline Total serum

aminotransferase aminotransferase Phosphatase bilirubin (mg/dl)
(IU/L) (IU/L) (IU/L)

Mean 26.2 35.7 365 3

Range 5-103 5-128 15-930 0.3-19

Normal range Up to 45 Up to 45 Up to 125 0.2-1.2

No. of patients with value more

9 (16.4%) 13 (23.6%) 39 (71%) 32 (58.2%)
than upper normal

Table 2. Alkaline phosphatase was the most likely parameter to be abnormal while aminotransferases were the least.

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More than two thirds of patients had high alkaline phosphatase and more than one half had abnormal total serum
bilirubin while less than one quarter had abnormal aminotransferases.

Parameter Trans-abdominal MRCP Computed Endoscopic

ultrasound Tomography ultrasound

No. of patients 55 (100%) 20 (36.4%) 12 (21.8%) 3 (5.5%)

Range of bile duct diameter 9-25 mm (12.4

(mean) 7-20 mm (9.8 mm) mm) 7-16 (10.7 mm) 10 mm (10 mm)

Stone / filling defects 15 (27.2%) 5 (20%) 3 (25%) 2 (67%)

Leak None 3 (15%) None None

Cut off / Missed segment None 6 (30%) None None

Collection 9 (16.4%) 1 (5%) 4 (33%) None

Table 3. Imaging studies of study population: Trans-abdominal ultrasound detected bile duct dilatation (62%) or stones (38%) in
patients with bile duct stones and collection (47%) in those with bile duct injury.

Trans-abdominal ultrasound was performed for all the cases while 20 patients had MRCP, 12 patients had CT scan
and only 3 patients had EUS. The findings on these imaging studies are shown in table-3 and included bile duct
dilatation, filling defects / stones, leaks, cut off/missed segment or collection. Of those who had stones on ERCP
(N=32), trans-abdominal ultrasound detected bile duct dilatation in 20 patients (62%) and stones in 12 patients
(38%). It detected collections in 9 (47%) of the 19 patients with bile duct injuries. MRCP could identify features of
bile duct injury (leak, cut off/missed segment or collection) in 52% while CT scan only confirmed the finding on
trans-abdominal ultrasound. Endoscopic ultrasound showed filling defects in 2 out of 3 cases (67%).

SN Findings No. Intervention Follow up Complications

ES ES + Stent ES + Improved Referred for Pancreatitis Cholangitis

Stent extraction surgery

1 Normal 1 0 0 0 0 1 0 1 0

Retained bile duct

2 32 2 6 0 24 30 2 2 0
stones

3 Extraction of parasites 3 0 0 0 3 3 0 0 0

Bile duct injury

4 19
(Bergman class)

4.1 A 10 0 9 0 0 9 1 0 0

4.2 B 3 0 3 0 0 2 1 0 0

4.3 C 2 0 1 1 0 1 1 0 1

4.4 D 4 0 0 0 0 0 4 0 0

Total 55 2 19 1 27 46 9 3 1

Table 4. Findings, interventions, follow up and complications of ERCP: The overall success rate for endoscopic intervention was
83.6% which was higher for stones (93%) compared with bile duct injuries (63%) with the success rate declining as the
Bergman class increases. Abbreviations: ES = Endoscopic Sphinecterotomy, ERCP= Endoscopic Retrograde Cholangio-
Pancreatography.

The most common finding on ERCP was retained bile duct stones (N=32, 58.2%) followed by bile duct injuries
(N=19, 34.5%) while parasites were extracted in 3 patients (5.5%). The overall success rate for endoscopic
intervention was 83.6%. This was higher for stones (93.7%) compared with bile duct injuries (63.2%) with the
success rate declining as the Bergman class increases. Nine patients (16.4%) were referred for surgery, 3 of these
died. The most common complication of ERCP was pancreatitis (N=3, 5.5%) as shown in table-4. There was a
significant statistical association between death and each of bile duct injuries, failure of endoscopic treatment and
referral for surgery (P <0.05). There was no significant statistical association between the type of cholecystectomy
and each of the patient’s sex, clinical presentation, laboratory data, findings on ERCP, success of ERCP
intervention or complications of ERCP (P > 0.05).

Discussion
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Cholecystectomy, which has been performed for more than a century, continues to carry a recognized spectrum of
complications that can affect the patient’s wellbeing and may result in death [1] [11]. The rate of these problems is
higher with the laparoscopic approach despite all the intraoperative measures taken to reduce them [3]. Therefore,
keeping vigilance and interfering as early as possible is important [4]. The currently available options for
intervention are surgery, ERCP and percutaneous trans-hepatic biliary drainage (PTBD). Surgery and PTBD are
associated with higher mortality and morbidity rates than those of ERCP which is gaining increasing popularity as
the modality of first choice in these conditions [12] [13]. Much of the acceptance in the current use of ERCP has
occurred without data from comparative trials. However, it is wise to conduct prospective trials to achieve the best
outcome from the use of ERCP [14].

Although laparoscopic cholecystectomy has become the standard of care for most gallbladder diseases [1], about
one third of cases (N=17, 31%) in this study underwent cholecystectomy with the open method. Many patients were
referred from district hospitals where the open approach is still used by surgeons who lack adequate training and
experience which also results in higher complications rates as well as lower ability to recognize and manage them
intra-operatively. This has been reported in other studies [3] and may further signify the importance of ERCP.

Most of the patients in this study were females younger than 50 years which is concordant with that reported by
other studies [3] [4] [7] [15]. Abdominal pain was the most common presentation in this study which is similar to
studies done by Singh et al [16] and Hassanien [17] while a study by Nawaz et al [3] reported jaundice as the most
common presentation followed by abdominal pain.

In our study, the laboratory test that was most likely to be abnormal was alkaline phosphatase followed by serum
bilirubin and then aminotransferases while the liver biochemical tests were normal in at least one third of patients.
Therefore, normal liver biochemical tests should not discourage us from carrying out more investigations especially
in suspected bile duct leaks [2] [17].

Trans-abdominal ultrasound detected bile duct dilatation (62%) or stones (38%) in patients with choledocholithiasis
and collection (47%) in those with bile duct injury compared to 76% [7], 50% [7] and 52% [4] respectively in other
studies while it was normal in 47% of all cases. Hence, a normal ultrasound should not preclude further evaluation.
CT scan was only able to confirm the findings of trans-abdominal ultrasound [1]. MRCP increased the sensitivity of
imaging to detect bile duct injury to 74% which is lower than the 95% rate reported in other studies [4].

From the above discussion, one can extrapolate that clinical features, liver biochemical tests and imaging cannot
reliably exclude post-cholecystectomy complications; hence, the role of ERCP in this regard. Retained bile duct
stones were identified in 58.2% compared to a range of 27% to 64% in other studies [3] [15] [18] [19]. They were
treated with endoscopic sphinecterotomy combined with stone extraction and / or stenting with the latter inserted for
large stones or to prevent cholangitis when complete clearance was not sure [9] and removed after 1 month.

The commonest type of bile duct injuries was peripheral leaks, mainly from the cystic duct, which is similar to other
studies [18] [19] [20]. Bile duct strictures were identified in 10.5% and complete transections in 21% which are
comparable to other studies, reporting rates of 2-31% for stricture and 10-25% for transections [3] [15] [18]. Bile
duct injuries were treated with stenting combined with endoscopic sphinecterotomy in all but one case to facilitate
sent deployment, a finding similar to other studies [3] [15]. Complete transections were referred for surgery as in
other studies [3] [4] [17]. Currently, the major role of ERCP in complete transections is diagnostic pending further
advances in therapeutic endoscopy to manage such problem.

Parasitic infestations were noticed in 3 patients (5.5%) including membranes of ruptured hydatid cysts in two
patients and a patient with Fasciola hepatica. This was combined with endoscopic sphinecterotomy and followed by
antiparasitic agents. Intrabiliary rupture of hepatic hydatid cyst is a well-recognized complication of hydatid disease
that is being increasingly treated with ERCP with success rates of 50% reported by another study done in our
center [21]. Fascioliasis is a zoonotic disease that was overlooked but is increasingly identified in Sulaimani
governorate and is attributed to raw watercress consumption in some rural areas [22]. Both of these parasitic
diseases are more likely to be missed from inadequate preoperative assessment. Only one person (1.8%) with
normal cholangiogram was reported in this study while other studies reported this in 3.4-11.2% [3] [11] [19].

The overall success rate for endoscopic intervention was 83.6% which is comparable to the published rates in the
range of 75-88% [3] [19] [23]. It was highest for retained bile duct stones (93.7%) and it is within the reported rates
of 88-100% [3] [7] [13]. For bile duct injury, the endoscopic intervention was successful in 63.2% with success rates
declining as the Bergman class increases (90% for class-A, 67% for class-B, 50% for class-C) compared to those
published by others with the overall success rate ranging 53-95% [11] [12] [16] [17] [24], while it is 95% for class-A,

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71-79% for class-B and 80-89% for class-C [9]. One of the two patients with bile duct strictures was referred for
surgery and proved on follow up to be a case of cholangiocarcinoma which was likely missed at the time of surgery
and the patient died after developing cholangitis. Cholangiocarcinoma was reported in other studies and should
always be considered when confronted with bile duct strictures [3] [11]. The endoscopic intervention failed in 16.4%
and these were referred for surgery which was more likely in bile duct injuries especially in Bergman class - D.
Other studies have reported referral rates for surgery in the range of 6 - 27% [3] [4] [11] [12].

The complications of ERCP in our study were pancreatitis (5.5%) and cholangitis (1.8%) which are comparable to
those reported in the literature with the rates of post-ERCP pancreatitis being 1.9-5.4% and those of cholangitis
being 1.4-1.7% [9]. All the cases of pancreatitis were mild and were treated conservatively without clinical
consequences.

The mortality rate was 5.5% (N=3). They had bile duct injuries and were not amenable for endoscopic intervention
with consequent referral for surgery. These three cases were cholangiocarcinoma missed at the time of
cholecystectomy, bile leak in an elderly with comorbidities and a case of complete transection. All of them had a
protracted post-operative course with sepsis and multi-organ system failure that culminated in death. The mortality
rates in other studies were in the range of 2-12.5% [24] [25].

The type of cholecystectomy (open versus laparoscopic) was not related to sex, clinical presentation, laboratory
data, findings on ERCP, success of ERCP intervention or complications of ERCP (P > 0.05). This indicates that
even if the laparoscopic approach has higher incidence of complications [3], the characteristics of these
complications and the success of endoscopic management is not influenced by whether the patient had undergone
laparoscopic or open cholecystectomy. This has been shown in various randomized controlled trials [26] although
recent large observational studies show that the laparoscopic approach is preferred to open method with regard to
short term complications [27].

The limitations of this study were the small sample size and the short period of follow up. Larger scale studies with
longer follow up periods are needed to confirm our findings.

Conclusion
The commonest post-cholecystectomy complications were retained bile duct stones followed by bile duct injuries.
ERCP is an effective and safe method in the diagnosis and management of these complications.

Declarations
Consent

Patients and their families were informed and a written consent was obtained. Copies of these consent forms are
available for review by the Editor-in-Chief of this journal.

Acknowledgments

We would like to thank Dr. Rekawt Hama Rasheed, Dr. Miran Mohammed Abbas and Dr. Ari Sami Hussain for their
support. We are grateful for our patients and their families for their adherence to the follow up period requirements.
We also thank Dr. Beston Faiek Nore for his advice regarding the style of the manuscript and Dr. Jabar Mohamad
Salih for revising the manuscript linguistically. Special thanks to the staff of KCGH for their kind help in collecting
data.

Authors’ contributions

SHSQ designed and coordinated the overall project. TAA did all the ERCP procedures. AAR analyzed data and
wrote the manuscript. HMA followed up the patients and gathered data. TAHH revised the manuscript. All authors
read and approve the manuscript.

Conflict-of-interest disclosure

The authors declare no competing financial interests.

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ISSN : 2334-1009

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