Outcomes of Laparoscopic Common Bile Duct Exploration After Failed Endoscopic Retrograde Cholangiopancreatography in Patients with Concomitant Gall Stones and Common Bile Duct Stones: A Prospective Study

Abstract

Introduction:

The aim of the present study was to compare the outcomes of secondary laparoscopic CBD exploration (LCBDE) following failed endoscopic retrograde cholangiopancreatography (ERCP) and primary laparoscopic common bile duct (CBD) exploration.

Materials and Methods:

One hundred eighty-five patients undergoing LCBDE were divided into Group I consisting of patients undergoing a primary LCBDE (n = 102) and Group II consisting of patients undergoing LCBDE after failure of ERCP to clear the CBD stones (n = 83). Primary outcome measure was successful laparoscopic CBD clearance. The secondary outcome measures were degree of difficulty, operative time, complications, hospital stay, and the cost of treatment.

Results:

Success rate was similar in both groups (85.3% versus 80.7%). Mean operative time, degree of difficulty, hospital stay, and cost of procedure were significantly higher in Group II (P value <.05).

Conclusion:

It may be prudent to consider ERCP failure patients for primary LCBDE than risk the complications of ERCP if they are suitable for primary surgery.

Introduction

The optimum management of patients with concomitant gallstones and common bile duct (CBD) stones is debatable. Endoscopic retrograde cholangiopancreatography (ERCP) followed by cholecystectomy is the preferred method of management at present, although randomized trials have shown single-stage cholecystectomy and laparoscopic CBD exploration (LCBDE) to be equally efficacious and safe when compared with endoscopic stone clearance followed by cholecystectomy. Few randomized trials have shown that single-stage treatment may be even superior to two-stage management in terms of patient satisfaction, hospital stay, and cost effectiveness.^1,2

ERCP, however, remains the standard of care for patients with complicated CBD stones, for example, those with cholangitis, pancreatitis, or patients with post cholecystectomy CBD stones.³ Although the success rate of endoscopic extraction of CBD stones may reach 90% or more, not all CBD stones are amenable to endoscopic stone clearance, for example, in patients with altered gastric or duodenal anatomy, large and impacted stones and/or concurrent biliary stricture.⁴ Successful clearance may still be achieved in such situations with the use of specialized procedures, for example, balloon sphincteroplasty, mechanical lithotripsy, and so on, but this requires multiple sittings increasing the cost and chances of complications, such as pancreatitis, bleeding, and cholangitis.⁴

Even then, there remains a group of patients in whom endoscopic extraction of stones fails. Such patients are referred for CBD exploration, but various studies have shown that CBD exploration may present the surgeon with certain technical difficulties due to multiple and impacted stones and the dense adhesions secondary to ERCP-induced bacterobilia, low-grade cholangitis and accompanying pericholedochal inflammation.^5,6 Few studies have shown successful stone clearance in post-ERCP patients undergoing laparoscopic CBDE for failed endoscopic stone extraction.

This present study was conducted with the aim to compare the outcomes and intraoperative difficulties of LCBDE following failed ERCP with primary LCBDE.

Patients and Methods

Patients having gallstones with concomitant CBD stones undergoing LCBDE in a single surgical unit were studied prospectively at a tertiary care hospital from January 2006 to May 2013. Ethical clearance was obtained from the Institute Ethics Committee. Patients were divided into two groups. Group I consisted of patients undergoing a primary LCBDE and Group II consisted of patients undergoing LCBDE after failure of ERCP (LCBDE after failed ERCP) to clear the CBD stones. Patients with gallstones and CBD stones who did not have any history suggestive of cholangitis, sepsis, or pancreatitis underwent single-stage treatment, whereas the second group included patients who were referred for CBD exploration after failure at ERCP for stone extraction.

Demographic details like age, sex, clinical features, cholangitis, acute pancreatitis, history of cholecystectomy, and comorbidities were noted. Complete hemogram, liver function tests (alanine transaminase, aspartate transaminase, bilirubin, alkaline phosphatase, and albumin), and prothrombin time were done. Findings of transabdominal ultrasound and ERCP were noted. An ERCP or magnetic resonance cholangiopancreatography (MRCP) was used for confirming the diagnosis of CBD stones and delineating biliary anatomy preoperatively in all patients. Reasons for failure of ERCP were noted. Intraoperative details like degree of adhesions, size of choledochotomy, number and size of stones, techniques used for stone extraction, mode of closure of bile duct, and level of difficulty of CBD exploration were noted. The postoperative recovery, complications, antibiotic usage, drain removal, and hospital stay were recorded.

Operative technique for LCBDE in brief is as follows and detailed procedure has been reported previously.^7,8 Patients were started on prophylactic broad-spectrum intravenous antibiotics at the time of induction. The antibiotics were continued for 48 hours and then switched to oral antibiotics depending on the clinical status of the patient.

The patient was placed in a supine position. Pneumoperitoneum was created using Veress needle supraumbilically. Five ports were used with 10 mm 30° telescope at the umbilicus. The position of the epigastric port was slightly different than in standard cholecystectomy: the epigastric port (12-mm Excel port; Ethicon) was inserted 2.5 cm to the right of midline so that the port was directly in the line of the CBD. Two working ports and an additional 5 mm port was placed in the left paramedian area just above the umbilicus for insertion of a choledochoscope (rigid) for visualization of upper tracts and closure of choledochotomy.

Dissection began around Calot's triangle, cystic duct and cystic artery were ligated/clipped, and gallbladder was partially dissected from its bed and used for retraction. A longitudinal supraduodenal choledochotomy was made using Endoknife (Karl-Storz). The stones and debris from the CBD were removed either by thorough flushing with a copious amount of normal saline or using forceps. Choledochoscopy was performed either using a flexible choledochoscope (11-French, 30°; Karl-Storz) or rigid nephroscope (6°, 17-French; Karl Storz) inserted through the epigastric port. Thorough visualization of the upper portion of CBD along with right and left hepatic ducts, secondary, and tertiary ducts was performed. Choledochoscope was then directed downward to visualize the lower part of the CBD up to the papilla. Any residual stones were removed using Dormia basket or Fogarty Catheter or Triflange forceps (through rigid nephroscope). Mechanical lithotripter was used to break impacted stones and the fragments were removed. A check choledochoscopy was done to ensure CBD clearance. Choledochotomy was closed using absorbable suture (4–0 Vicryl; Ethicon) either primarily or over a T-tube/endobiliary stent.

In patients with a T-tube, a T-tube cholangiogram was done after 5–7 days to document CBD clearance and patency. The T-tube was removed after 2–4 weeks if there were no retained stones and there was free flow of contrast across the ampulla. Patients were followed up at 1 week, 6 weeks, 3 months, 6 months, and annually thereafter. Liver function tests were obtained at each visit and abdominal ultrasound at 6 weeks, and repeated if patient developed symptoms like pain, fever, or jaundice.

Outcomes

Primary outcome measure was successful laparoscopic CBD clearance. The secondary outcome measures were need for conversion, degree of adhesions and difficulty of exploration, operative time, complications, and hospital stay. The operative surgeon graded the degree of adhesions into four grades as none, mild (flimsy, avascular adhesions; separate easily with blunt dissection), moderate (firm, limited vascular adhesions; separate with sharp dissection), and severe (fibrotic, dense, vascular adhesions; separate with sharp dissection). The difficulty of CBD exploration was rated as “easy,” “not easy,” or “difficult” based on the assessment of the operating surgeon. Two senior laparoscopic surgeons performed all the surgeries.

Statistical analysis

Statistical analysis was performed using SPSS for Windows (SPSS, Inc., Chicago, IL). Unpaired Student's t-test was used to determine the significance of difference between the two independent groups for continuous variables. For skewed data, Mann–Whitney test was applied. For qualitative data, Chi-square test was used to see the significant difference in proportion between the two groups. Significance was set at 5% level and a P value <.05 was taken as significant.

Results

One hundred eighty-five patients underwent LCBDE during the study period. Of these, 102 patients underwent primary laparoscopic CBDE (Group I) and 83 patients underwent laparoscopic CBDE after failed ERCP (Group II).

The demographic profile was comparable between the two groups (Table 1). Patients undergoing LCBDE after failed ERCP had significantly higher incidence of jaundice and cholangitis as compared with patients undergoing primary LCBDE. Patients in this group also had significantly higher total leukocyte counts and serum bilirubin levels.

Table 1.

Comparison of Demographic, Clinical, and Laboratory Parameters

	Group I (n = 102)	Group II (n = 83)	P
Age (years), mean ± SD (range)	45.8 ± 14.2 (10–74)	47.8 ± 15.2 (19–82)	.8
Sex, n (%)
Male	27 (26.5)	24 (28.9)	.7
Female	75 (73.5)	59 (71.1)
BMI (kg/m²), mean ± SD (range)	24.8 ± 3.9 (12.8–34.2)	22.5 ± 3.5 (15.1–29.0)	.3
Jaundice, n (%)	47 (46.1)	64 (76.1)	<.001
Past history of cholangitis, n (%)	22 (21.6)	48 (57.8)	<.001
Past history of pancreatitis, n (%)	0 (0)	3 (3.6)	.08
TLC (cells/mm³), mean ± SD (range)	7724.3 ± 2094.1 (4600–15700)	10128.3 ± 4824.5 (3100–26500)	<.001
T. bilirubin (mg %), mean ± SD (range)	2.4 ± 2.8 (0.4–15.7)	6.2 ± 5.4 (0.3–27)	<.001
SGPT (IU/dL), mean ± SD (range)	75.2 ± 66.7 (8–361)	80.5 ± 100.3 (10–764)	.8
Alkaline phosphatase (IU/dL), mean ± SD (range)	625.5 ± 601.4 (132–4390)	590.3 ± 368.9 (120–1788)	.5

Significant values are shown in bold.

BMI, body mass index; SD, standard deviation; TLC, total leucocyte count; SGPT, serum glutamic pyruvic transaminase.

The causes of ERCP failure were multiple or large impacted stones in 67 patients (80.7%), failure to cannulate papilla in 6 patients (7.2%), nonvisualization of stone in 5 patients (6%), Mirizzi's syndrome in 3 patients (3.6%), impacted stent with stones in 1 patient (1.2%), and intrahepatic stones in 1 patient (1.2%).

Outcome measures

Patients undergoing primary LCBDE had a higher successful CBD clearance (85.3%) as compared with LCBDE after failed ERCP (80.7%), but this was not statistically significant (odds ratio 1.38, confidence interval 0.64–3.0; Table 2). The reasons for conversion were similar between the two groups.

Table 2.

Comparison of Success and Intraoperative Parameters

	Group I (n = 102)	Group II (n = 83)	P
Success	87/102 (85.3%)	67/83 (80.7%)	.4
Mean operative time (minutes), mean ± SD (range)	130.2 ± 38.7 (75–240)	144.3 ± 44.4 (60–240)	.02
Mean choledochotomy size (cm), mean ± SD (range)	1.5 ± 0.4 (0–2)	1.6 ± 0.4 (0–2)	.43
Stone size, n (%)			<.001
Small	29 (28.4)	7 (8.4)
Medium	39 (38.2)	17 (20.5)
Large	33 (32.3)	53 (63.9)
Choledochotomy closure, n (%)			<.001
Primary	69 (67.6)	35 (42.2)
Internal stent/NBD	2 (2.0)	27 (32.5)
T tube	28 (27.5)	19 (22.9)
Median duration since ERCP (weeks)	NA	6 (1–104)
Ease of surgery, n (%)			.006
Easy	28 (27.5)	10 (12.1)
Moderately difficult	42 (41.2)	30 (36.1)
Very difficult	32 (31.3)	43 (51.8)
Adhesions, n (%)			.004
Minimal	6 (5.9)	6 (7.2)
Mild	47 (46.1)	17 (20.5)
Moderate	24 (23.5)	28 (33.7)
Severe	25 (24.5)	32 (38.6)

Significant values are shown in bold.

ERCP, endoscopic retrograde cholangiopancreatography; NBD, naso billiary drainage.

Majority of the patients underwent direct choledochotomy (95%) and had multiple stones in the CBD (65.9%). The mean size of the supraduodenal choledochotomy was 1.5 cm, which was similar in both the groups. Patients undergoing LCBDE after failed ERCP had significantly larger CBD stones (more than 1 cm) as compared with patients undergoing primary LCDBE (63.9% versus 32.3%, P < .001). Check choledochoscopy was done to confirm CBD clearance.

Primary CBD closure was done in more patients (67.6% versus 42.2%) following primary LCBDE as compared with LCBDE after failed ERCP, which was statistically significant (P ≤ .001). Three patients underwent choledochoduodenostomy as a drainage procedure after primary LCBDE and two patients underwent a hepaticojejunostomy for recurrent and impacted stones as a drainage procedure after LCBDE after failed ERCP.

Patients undergoing LCBDE after failed ERCP had significantly more severe adhesions (38.6% versus 24.5%, P = .004), a difficult Calot's Triangle LCBDE (66.3% versus 45.1%, P = .004) and a difficult cholecystectomy (48.6% versus 21.2%, P = <.001). The surgery was overall graded as more difficult in this group (51.8% versus 31.3%, P = .006) as compared with patients after primary LCBDE (Table 2).

The mean operative time was also significantly longer after failed ERCP LCBDE (144.3 ± 44.4 versus 130.2 ± 38.7 minutes, P = .02; Table 2). A subhepatic drain was placed in all the patients and removed after a median of 3 and 4 days. Patients undergoing LCBDE after failed ERCP also had a significantly longer hospital stay (4 days [2–15 days] versus 5 days [3–71 days], P = .003) and a higher antibiotic usage.

The incidence of postoperative complications were slightly higher in patients undergoing LCBDE after failed ERCP (34.9% versus24.5%, P = .2; Table 3). Transient bile leak was present in 15 patients in Group I and 12 patients in Group II. Although no intervention was required for bile leak, it prolonged the patients' hospital stay. This transient bile leak could be explained by the CBD wall edema that develops following surgical manipulation. As the time went by, this edema subsided and the transient bile leak stopped without any intervention.

Table 3.

Comparison of Postoperative Outcomes

	Group I (n = 102)	Group II (n = 83)	P
Complications, n (%)	25 (24.5)	29 (34.9)	.2
Transient bile leak, n (%)	15 (14.7)	12 (14.5)	.9
SSSI, n (%)	9 (8.8)	11 (13.3)	.5
Organ space infection	0	0
Acute pancreatitis	0	0
Perforation	0	0
Bleeding, n (%)	0	2 (2.4)	.4
Cholangitis, n (%)	0	1 (1.2)	.5
Mortality, n (%)	1 (0.9) (POD 3)	1 (1.2) (POD 12)	1.0
Antibiotic requirement (days)
Parenteral	3.2 ± 1.9 (1–18)	3.5 ± 3.6 (2–20)	.006
Oral	5.1 ± 0.9 (3–10)	6.1 ± 3.0 (5–20)	.04
Median hospital stay, days (range)	4 (2–15)	5 (3–71)	.003
Total cost per patient, Rs.	28476 ± 8359.7 (16445–59015)	37043.7 ± 29998.8 (18785–208055)	.006
Median duration of follow up (months)	11.4 ± 3.9 (6–24)	13.2 ± 3.4 (3–36)	.3
Retained stones, n (%)	3 (2.9)	0	.3

Significant values are shown in bold.

SSSI, superficial surgical site infection; POD, postoperative day.

The incidence of surgical site infection was comparable between the two groups (8.8% versus 13.3%, P = .5). Two patients each developed burst abdomen and bleeding in Group II. One patient had bleeding from liver bed, which was controlled with use of cautery on re-exploration and patient was discharged after 2 weeks. The other patient had oozing from the omentum that was adherent in the gallbladder fossa, which was controlled, but he again had to be re-explored for bleeding after 2 days. On re-exploration there was generalized oozing. Hemostasis was secured and patient was kept on ventilator in view of massive blood loss and sepsis. She however developed ventilator-associated pneumonia and succumbed to sepsis. She was found to have adenocarcinoma of the gallbladder on histopathology report. One patient in the primary LCBDE group developed fulminant cholangitis in the immediate postoperative period and died within 72 hours despite aggressive antibiotic therapy. No autopsy was performed in any of these mortalities.

All patients were followed up for a median duration of 12 months (6 weeks to 4 years). Three patients were diagnosed with retained stones during follow up after primary LCBDE, and all 3 of them underwent successful ERCP and stone clearance. One patient in Group II was diagnosed as having carcinoma of the gallbladder on the postoperative histopathology and underwent a completion radical cholecystectomy and adjuvant chemoradiotherapy, and is doing fine on a follow-up of 24 months. There have been no long-term complications like CBD stricture or recurrent stones in any of the patients in both the groups.

Discussion

Ever since the advent of ERCP in 1970s, the treatment of CBD stones fell into the domain of gastroenterologists as ERCP had lesser complications and morbidity as compared with open CBD exploration.⁹

With increasing expertise in laparoscopic surgery and instrumentation, LCBDE has fast gained momentum and at present LCBDE has become the preferred treatment in many centers. Several randomized trials have shown feasibility and success of LCBDE over ERCP followed by laparoscopic cholecystectomy.^1,2,9. We have also shown recently in a randomized controlled trial that both LCBDE and endoscopic therapy were similar for CBD stones, although the complications and costs were higher in the endoscopic group.⁷ However, ERCP continues to have a definite primary role in the management of CBD stones especially in postcholecystectomy CBD stones and in patients with acute cholangitis or acute pancreatitis. The area of controversy continues to be patients with gallstones and CBD stones with CBD >10 mm and no active cholangitis. Our present study, as well as the previous study⁷ have shown that primary CBD exploration in this situation is not only more cost effective, but also associated with significantly lesser postoperative complications. Also any laparoscopic procedure (lap cholecystectomy or LCBDE) following ERCP is more difficult and has higher postoperative complication rate. Thus patient presenting with concomitant gallstones with CBD stone with CBD >10 mm without active cholangitis may be offered the advantages of a primary CBDE rather than ERCP followed by laparoscopic cholecystectomy.

ERCP may be unsuccessful in 4%–25% of patients with CBD stones.¹⁰ The causes of failure of ERCP include large periampullary diverticulum, altered anatomy or failure of stone extraction due to multiple or large impacted stones, intrahepatic stones, etc.¹¹

The presence of multiple or large stones is one of the most common causes of ERCP failure^4,11 as also observed in the present study. A study conducted in our institution by Garg et al.¹² showed that the success rate reduced from 90% to 79% when the stones were impacted, which was also a major cause of failure of mechanical lithotripsy. Multiple attempts and maneuvers required for CBD clearance in these patients increase the risk of complications, such as pancreatitis, bleeding, and perforation.¹³

The stone size and impaction, unlike in endoscopic stone extraction, is not an important predictor of failure for LCBDE. In the present study, 94% of patients referred for removal of impacted stones could be cleared by LCBDE with only 4 patients requiring conversion for impacted stones. Other studies have also shown clearance rates ranging from 70% to 100% for removal of impacted stones by laparoscopy. We were able to clear the impacted stones using mechanical lithotripter in majority of the cases.

Many studies have shown that laparoscopic cholecystectomy may become difficult after ERCP. It is well known that bile is infected with bacteria after disruption of Oddi's sphincter by sphincterotomy and stone extraction during ERCP.¹² The infection of the bile could be the initiator of inflammation in and around the bile duct and gallbladder with unpredictable adhesions and altered anatomy, which increases the difficulty of both laparoscopic cholecystectomy and LCBDE.^14–17 However, this aspect has not been studied in patients undergoing LCBDE.

The success rates of laparoscopic exploration of the CBD following prior attempts at ERCP range from 64.5% to 97.7%.^18–22 Only a few retrospective studies and one prospective study have compared the outcomes of LCBDE after unsuccessful ERCP with primary LCBDE. In the present study, we have found that the CBD exploration after previous ERCP had a slightly lower success rate, but this difference was not statistically significant. These findings are also in accordance with Tai et al.²⁰ who also reported similar clearance rates in both the groups. Similar results were also shown by Karaliotas et al.¹⁹ and Paik and Kim²² This is in contrast to the findings of Sanchez et al.²¹ who found higher rates of conversion in the ERCP-failed CBD stones. However, these studies are retrospective with small sample size with the possibility of type II error.

It is well known that bile is infected with bacteria after disruption of Oddi's sphincter by sphincterotomy and stone extraction during ERCP, which initiates inflammation in and around the bile duct and gallbladder.¹⁴ Additionally, the presence of a foreign body in the biliary system has been proven to facilitate bacterial adhesion and biofilm formation.²³ This low-grade infection along with the presence of a stent leads to persistent inflammation and fibrosis of the structures in the extrahepatic bed.²⁴

We found that in the post-ERCP CBD explorations, there were significantly greater adhesions making it difficult to define the anatomy (Calot's Triangle). Furthermore, the presence of multiple and impacted stones adds to the technical challenge. All these factors led to an overall increase in the difficulty of surgery in patients undergoing LCBDE after failed ERCP.

Majority of our conversions in patients with failed ERCP were due to either dense adhesions or unpredictable anatomy. Karaliotas et al.¹⁹ also had to convert due to dense adhesions in 36% of patients in their study. Paik and Kim²² also had one conversion in their study, which was also due to dense adhesions. Similar observations were made by Allen and Leeth¹⁵ and Donkervoort et al.¹⁶ who showed that laparoscopic cholecystectomy after ERCP has higher rates for complications and conversion caused by unpredictable adhesions.

The mean operative times in the patients undergoing CBD exploration following failed ERCP was significantly longer due to dense and unpredictable adhesions, and presence of multiple large stones. This was also observed in studies by Tai et al,²⁰ Paik and Kim,²² and Sanchez et al.,²¹ also showing significantly prolonged operative times in patients undergoing LCBDE following failed ERCP.

The incidence of bile leak was found to be comparable between both the groups. In all patients, the bile leak was only transient and did not require any intervention in any of these patients. We expected the patients who had undergone preoperative stenting to have a higher incidence of wound-related complications as the bile is usually not sterile in the presence of an indwelling prosthesis, but we found the incidence of infectious complications to be comparable. Our incidence of wound infection following LCBDE is nearly the same as reported in the literature (0.5%–4%).⁶ Similar results were observed in the other studies also with comparable rates of complications between both the groups.^11,19

The median hospital stay of patients undergoing LCBDE following failed ERCP was significantly prolonged in comparison to those undergoing primary LCBDE. This is in contrary to the existing literature, which shows the hospital stay to be comparable between the two groups.^20–22 This was because we found that majority of patients developed low-grade biliary sepsis in the immediate postoperative period, probably from reflux of infected bile during surgery, requiring antibiotic support and in-hospital observation, which was also evident from the higher requirement of antibiotics in these patients as compared with those undergoing primary LCBDE, thereby leading to a longer hospital stay. This increased hospital stay along with increased operative time led to a significantly higher cost of treatment. This further emphasizes the need for LCBDE to be performed as a primary procedure for patients with concomitant gallstones and CBD stones without complications, rather than as a salvage procedure after failure of endoscopic stone extraction. This study also highlights the fact that patients with no active cholangitis or pancreatitis and having large CBD stones should undergo a direct LCBDE rather than a ERCP first because the chances of success in direct LCBDE is higher as compared with ERCP.

Conclusion

For patients with multiple or large impacted CBD stones, ERCP has a significantly higher failure rate, sometimes requiring multiple procedures for achieving ductal clearance. Although the conversion rates, complications, and postoperative outcomes of patients undergoing LCBDE after failed ERCP are similar to those undergoing a primary LCBDE, LCBDE is more difficult, with greater adhesions, requiring longer operative times, longer hospital stay, and at a greater cost. It would therefore be prudent to consider such patients with large impacted stones for primary LCBDE rather than risk the complications of ERCP if they are suitable for primary surgery, especially in centers where expertise in laparoscopic surgery is available with the required operative setup. It is also necessary to develop programs for training of surgeons in LCBDE.

Footnotes

Authors' Contributions

V.K.B.—study concept and design and all surgical procedures; critical revision of manuscript for intellectual content and flow of the manuscript. A.K.—drafting of the article; critical revision of the article for important intellectual content; statistical analysis. K.R.—acquisition of data; analysis and interpretation of data. O.P.—acquisition of data; analysis and interpretation of data. S.K.—drafting of the article; critical revision of the article for important intellectual content. S.R.—drafting of the article; critical revision of the article for important intellectual content; statistical analysis. P.G.—study concept, design, and all endoscopic procedures and follow-up of patients. M.C.M.—revision of the article for important intellectual content; statistical analysis.

Disclosure Statement

No competing financial interests exist.

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