Clinically, 9% to 20% of cholecystectomies are complicated by choledocholithiasis.1,2 Although up to one-half of the cases are asymptomatic, gallbladder stones (GBS) with choledocholithiasis are responsible for some severe complications, such as acute obstructive suppurative cholangitis and pancreatitis, and result in considerable morbidity and mortality.3 The extraction of common bile duct stone (CBDS) is, therefore, the primary object of the treatment. Current treatment methods comprise both 1-stage and 2-stage procedures. The 2-stage procedure, which entails either preoperative endoscopic retrograde cholangiopancreatography (ERCP) or endoscopic sphincterotomy (EST) followed by laparoscopic cholecystectomy (LC), has for long been considered as the optimal treatment.4 Today, many new options are available for the 1-stage procedure too, such as the combination of LC with intraoperative endoscopic sphincterotomy (IOEST) or laparoscopic common bile duct exploration (LCBDE) with T-tube drainage (TTD). Despite the continuous development of new surgical methods for the treatment of concomitant CBD stone and GBS, the optimal approach has not been established so far.5
To establish optimal treatment protocols for patients, most surgeons select LCBDE as compatible management for CBDSs at the beginning of 1-stage LC6 with TTD as a traditional part as suggested by the UK guidelines.7 However, a Cochrane systematic review by Gurusamy et al8 suggested that TTD should not be a routine step in LCBDE because of its complications. Although a final consensus has not been obtained to date, some surgeons began to perform primary duct closure (PDC) after LCBDE.9 However, PDC without drainage is responsible for severe postoperative complications, of which bile leakage is the most common one.10 To achieve a balance between the reduction of complications achieved by TTD and taking full advantage of PDC, Lv et al11 used intraoperative endoscopic nasobiliary drainage (IO-ENBD) when replacing TTD with PDC in LCBDE. In contrast, many surgeons turned to LC with IOEST to eliminate LCBDE-related complications. However, EST still carries a considerable risk of bleeding, perforation, and pancreatitis.12 Furthermore, it is inconvenient to perform laparoscopic and endoscopic surgery combined with intraoperative cholangiography (IOC) in one operating room, let alone carrying and arranging the endoscopy and radiologic equipment.
In recent years, a hybrid procedure that combines the standard surgical and radiologic treatment has been adopted in neurosurgery and vascular surgery and shows substantial benefits and efficacy.13,14 However, a hybrid method that combines laparoscopic surgery with endoscopic and radiologic treatment has not yet been developed in hepato-pancreatico-biliary surgery. In 2015, we introduced a 1-stage hybrid procedure that combined surgical (LC and LCBDE with PDC), endoscopic (IO-ENBD), and radiologic techniques (IOC) in the treatment of GBS with concomitant CBDS. In this study, we present the short-term clinical outcomes of this new procedure and share our preliminary experience.
MATERIALS AND METHODS
In this retrospective study, we reviewed the medical files of patients undergoing LC at our department from March 2015 to October 2017.
Inclusion and Exclusion Criteria
Patients diagnosed with GBS complicated with CBDS by either magnetic resonance cholangiopancreatography (MRCP) and/or B-type ultrasonography (BUS) were included in this study. The exclusion criteria were confirmed intrahepatic stones and acute obstructive suppurative cholangitis. After applying these criteria, a total of 47 patients were enrolled in the study.
Patient’s Baseline Data
Patients’ assessment included laboratory data and findings on clinical examination. The baseline data of the patients in this study are shown in Table 1. Their mean (±SD) age was 53.15±8.36 years (range, 27 to 74 y). The mean preoperative serum aspartate aminotransferase (AST) was 197.25±8.69 U/L, and AST was >40 U/L in 35 (74.47%) patients. The mean total bilirubin was 42.41±3.53 mol/L and >20 μmol/L in 22 (46.80%) patients. Eight (17.02%) patients had acute pancreatitis at the time of admission, and 4 (8.51%) patients were diagnosed with acute cholangitis. Fourteen (29.79%) patients had a history of abdominal surgery [2 patients had LC, 1 patient had 2 operations (open cholecystectomy and CBD exploration), 1 patient had undergone abdominal exploration and intestinal repair after a traffic accident, and 10 patients had a cesarean section]. Symptoms such as abdominal pain, especially in the hypochondrial region (19.14%), jaundice (14.89%), and fever (10.64%) were found in a total of 21 patients and treated with antibiotics on the basis of a regular blood test preoperatively.
The diameter of the CBD was assessed by MRCP and/or BUS.
Informed consent was obtained from all patients after a thorough discussion with them on the benefits and risks of the procedure.
Hybrid Procedure Combined With Tri-endoscopic Technique and IOC
LC was performed with 3 trocars under general anesthesia. Prophylactic antibiotics were given to all patients 0.5 hours before the operation. Patients were placed supine in a reverse Trendelenburg position of about 15 degrees on a radiolucent operating table to allow intraoperative C-arm imaging. After dissecting and clipping the cystic artery, we placed another absorbable clip on the cystic duct adjacent to its junction with the CBD to prevent stones from entering into the CBD. Then, the fourth trocar was inserted underneath the right subcostal line. The gallbladder was temporarily pulled into the right upper abdomen to ensure the better vision of the CBD.
A longitudinal choledocotomy of ~5 to 6 mm was made on the anterior wall of CBD, and a choledochoscope (Olympus CHF-T20 or P60; Olympus Corp, Tokyo, Japan) was inserted through it. After retrieving the stones with a basket (NTSE-045065-UDH; Cook Medical LCC, Bloomington, IN; Fig. 1), a duodenoscope was introduced into the second part of the duodenum by an endoscopist. A zebra guide wire (MTW-0.027; MTW-Endoskopie W. Haag KG, Wesel, Germany) was then inserted through the choledochoscope to pass the major duodenal papilla and pulled out through its hydrophilic tail (Fig. 2) by a choledochoscopy after finding it under duodenoscope with grasping forceps. An ENBD tube (8.5F; Wilson-Cook Medical Inc, Winston-Salem, NC) was inserted into the CBD guided by the zebra wire (Fig. 3). The position of the ENBD was adjusted according to the junction of the left and right hepatic duct during the operation (Fig. 4).
PDC was performed with either an interrupted suture or interrupted figure 8 suture using an absorbable 4-0 line (Fig. 5). After that, IOC was carried out through the ENBD to confirm that the CBD was free of stones and the ENBD properly positioned (Fig. 6). In the case of residual stones, the CBD was reopened, and stone extraction performed again with the choledochoscope until the IOC was negative. Afterwards, the cystic duct was transected and the gallbladder was removed from the hepatic bed. A drainage catheter was inserted in all patients to drain exudate from the gallbladder bed. All of the procedures were performed in a hybrid theatre (Fig. 7). Operation time was recorded from the incision of the first puncture to the final sewing of the incision. Stone characteristics were recorded by BUS preoperatively or by a vernier caliper postoperatively.
The duration of hospital stay, time until ENBD withdrawal, and the levels of total bilirubin and AST were recorded. The primary outcomes, including postoperative complications together with the secondary outcomes such as stone recurrence and CBD stricture, were analyzed postoperatively.
The success of the operation was defined as no conversion to open surgery and no residual stones in the CBD during IOC.
Complications associated with the operation included pancreatitis, cholangitis, bleeding, and bile leakage. Postendoscopic pancreatitis (PEP) was diagnosed in case of abdominal pain accompanied by serum lipase and/or amylase concentrations of at least 3 times the normal upper limit 24 hours after ERCP.15 Fever over 38°C continuing for 24 hours with cholestasis was diagnosed as cholangitis.16 Melena, hematemesis, or a decrease in hemoglobin postoperatively was considered as procedure-related bleeding.
The follow-up period was defined as the time from the date of discharge to the date of the last visit to the outpatient clinic. All of the patients in this study were notified to visit the outpatient clinic after 1, 4, and 7 months, and then every 6 months thereafter.
Quantitative data are presented as mean±SD and were analyzed using the Student t test. Statistical significance was set at P<0.05. Statistical analysis was performed using SPSS Statistics for Windows version 11.5 (SPSS Inc, Chicago, IL).
The success of the operation was defined as completion of the hybrid procedure, and no residual stones in the CBD detected by IOC after the operation. We completed the procedure without conversion to open surgery in 46 of the 47 cases (97.87%). In one patient, we found cholangitis with an oedematous CBD wall. The thickness of the wall was >3 mm, so we inserted a T-tube in case of a possible bile leakage postoperatively. No case showed residual stones postoperatively (Table 2).
The average duration of the procedure was 103.15±8.36 minutes. The number of stones varied from 1 to 6 (2.50±0.81). The diameter of the biggest stone was 1.9 cm, whereas that of the smallest one was 0.5 cm. All of the patients showed a widened CBD at an average diameter of 1.47±0.25 cm compared with normal values (Table 2).
IOC showed residual stones in the CBD in 4 patients (6.38%) after completion of PDC.
The average hospital stay was 6.37±1.28 days, and ENBD tubes were removed after 1.13±0.07 days. The mean level of AST 28.97±7.05 U/L and total bilirubin 14.82±1.21 μmol/L 3 days postoperatively showed a significant difference when compared with the preoperative data (P<0.05). Bile leakage was observed in 1 patient (2.13%). The bile was drained through a drainage tube, which was placed beside the omental foramen. The leakage ceased spontaneously after 3 days. One patient (2.13%) had postoperative cholangitis, which was treated with antibiotics and choleretic drugs (ademetionine). Two patients (4.26%) developed pancreatitis and recovered with somatostatin and proton pump inhibitor treatment. No patients experienced bleeding, stone recurrence, or stricture of the CBD related to biliary events during the follow-up period (Table 3).
Biliary stones (GBS or CBDS) may lead to cholecystitis, cholangitis, a liver abscess, or acute pancreatitis.3,17 There are different methods and procedures to remove stones, such as open choledocholithotomy, ERCP/EST, and laparoscopic surgery. ERCP/EST is still a popular procedure to treat CBD stones. According to the American Society for Gastrointestinal Endoscopy Criteria,18 the complications related to ERCP/EST are associated with morbidity ranging from 3.7% to 24%, consisting mostly of PEP, cholangitis, perforation, bleeding, and recurrent CBDS but also of cholangiocarcinoma in the long term.12,19 Therefore, it is recommended that EST should be limited to cases with adequate indications on the basis of accurate diagnostic tools.
With the advancement of laparoscopic surgery, 1-stage procedures, especially LCBDE, have made it possible to spare patients the drawbacks of 2-stage treatment.20 The European Association for Endoscopic Surgery21 recommends a single-stage laparoscopic treatment as a better option. The use of T-tubes in LCBDE remains controversial nowadays. On the one hand, it might decompress the biliary tract and offer access to the bile duct in case of postoperative residual stones. On the other hand, for patients, it could mean 2 to 4 weeks of pain and longer hospital stays. For surgeons, it means a significantly longer operating time because of the higher demand on their surgical skill [WMD, −24.82; 95% confidence interval (CI), −27.48 to −22.16] when compared with PDC.22 Some meta-analyses showed more complications associated with T-tubes than PDC, such as bile duct strictures, local pain because of the indwelling T-tube, and bile leakage caused by early T-tube removal.23,24 However, PDC is still a technically demanding skill with a relatively high risk of bile leakage, regardless of its broad use. In a meta-analysis, Liu et al10 found that a narrow CBD [odds ratio (OR), 95%; 95% CI, 1.081-13.349] and inexperienced surgeon (OR, 95%; 95% CI, 1.330-13.438) were risk factors for bile leakage after PDC. It seems that, as surgeons, we are facing a new problem: how to exploit the advantage of PDC fully while reducing its complications?
To solve this problem, we tried to substitute LCBDE with EST and replace TTD with IO-ENBD after PDC. ENBD is an optimal method to decompress the biliary tract and prevent pancreatitis after ERCP.25,26 It seemed that ENBD remained a 2-stage procedure, even though it represented a major step forward. In this study, we used a 1-stage hybrid procedure combining surgical, endoscopic, and radiologic techniques. Unlike in ERCP, in IO-ENBD, the hydrophilic end of the zebra guide wire enters the CBD through choledochoscopy, passes the sphincter of Oddi (SO), and travels into the second part of the duodenum in an antegrade manner. It is held with ease by grasping forceps through the duodenoscope. Under its guidance, an ENBD tube can be smoothly inserted into the CBD. Less injury to the duodenal papilla ensures a lower risk of bile leakage and PEP. However, the result was ambiguous: the bile leakage rate of 2.13% was encouraging compared with the one of 5.78% in another report,11 but at the same time, we observed a higher rate (4.26%) of PEP than the 0% in Lv et al’s study.11
Why did the hybrid procedure in our study show a relatively low bile leakage rate but a higher PEP rate? There are 3 procedure-associated risk factors, according to the European Society of Gastrointestinal Endoscopy (ESGE) guidelines.27 They are a cannulation time duration of >10 minutes (OR, 1.76), >1 pancreatic guide wire passage (OR, 2.77; 95% CI: 1.79-4.30), and pancreatic injection (OR, 2.2; 95% CI, 1.60-3.01). Theoretically, IO-ENBD can reduce or even prevent all these 3 factors, but, in fact, we found that the 2 cases who had PEP underwent >1 catheterization. In both, we did face no difficulty in ENBD catheterization initially, but when we released the laparoscopic forceps, the tube slid into the descending duodenum, and we had to repeat the catheterization. Therefore, we think that cooperation and coordination between surgeons and endoscopists are critical to complete the hybrid procedure successfully. The surgeons should pull the ENBD cranially upon seeing it in the CBD, and the endoscopists should push it simultaneously upwards. In addition, it is better when the endoscopists push the tube 2 cm further after having placed it in the optimal location (near the junction into the left and right hepatic bile duct) to relieve any tension. It seems reasonable to anticipate that, with the advancement of surgical suture skills and better cooperation of surgeons and endoscopists, biliary leakage and PEP could both achieve the aim of 0%.
Injury to the SO may lead to stenosis and prevent it from functioning as a natural barrier. The reflux of duodenal contents into the biliary tree results in bacterial colonization and recurrent stones after sphincterotomy.28,29 Cheon et al30 found that the basal pressure of the SO dropped from 30.4 to 6.4 mm Hg 1 week, and the SO function did not recover until 1 year after EST. In addition, though there is no high-level evidence that bacterial translocation after EST causes cholangiocarcinoma, there is some evidence that it causes proliferative changes in the CBD.31 With IO-ENBD and LCBDE, the SO function is protected. Consequently, neither CBD strictures nor stone recurrence occurred in our study.
IOC is particularly effective in detecting residual stones during LCBDE.32 In our study, 4 (6.38%) patients were found to have residual stones, and we explored the CBD again until the IOC showed a negative result. We think it is possible that a wide diameter of the CBD (in one case, it was 2.7 cm) together with the rapid flushing of NS from the choledochoscope causes the stones to float in the CBD and be overlooked. Therefore, the IOC is critical to ensure that no residual stones remain during the operation and avoids the risk of stone extraction postoperatively.
In summary, the preliminary results in this retrospective study suggest that the hybrid procedure combined with tri-endoscopic and radiologic techniques is feasible and safe for LC complicated with choledocholithiasis. It is necessary to carry out larger randomized controlled trials to prove its safety and effectiveness and to compare it with LCBDE and PDC and with LC and IOEST.
The authors appreciate the great help of Dr Li, Professor Fu, and technician Zhang in the GI unit during ENBD catheterization and IOC.
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