According to research results from different centers around the world, common bile duct (CBD) stones are detected in approximately 5 to 21% of patients undergoing surgery for symptomatic gallbladder stones [1]. CBD stones can result in biliary colic, obstructive jaundice, hepatic abscess, acute cholangitis, and pancreatitis. Traditional surgical treatment comprises intraoperative cholangiography to detect the presence of bile duct calculi followed by choledocholithotomy and T-tube placement [2]. Currently, endoscopic retrograde cholangiopancreatography (ERCP) and laparoscopic CBD exploration (LCBDE) are the most well-known, minimally invasive treatment options [3]. ERCP has remained the preferred invasive approach for managing symptomatic CBD stones for decades. However, ERCP always requires a two-stage approach (ERCP before or after laparoscopic cholecystectomy (LC)), although an increasing number of clinical centers try to perform ERCP during an operation. In addition, ERCP can sometimes cause serious ERCP-related complications, such as bleeding, duodenal perforation, cholangitis, and pancreatitis. Moreover, it may be difficult or impossible to clear large, multiple, intrahepatic ducts or impacted stones in the CBD by ERCP, and patients with these symptoms can benefit from open CBD exploration (OCBDE) or LCBDE, as these procedures have a high success rate in salvaging such stones [4]. In addition, it has been reported that endoscopic sphincterotomy (EST) may cause duodenobiliary, pancreatic juice and intestinal content reflux that results in recurrent bile duct stone formation, cholecystitis, inflammation in the bile duct, and cholangiocarcinoma [5]. Currently, some experts also suggest that ERCP be applied with appropriate indications in clinical practice.

For decades, laparoscopic skills have undergone considerable development. Since LCBDE was first introduced in 1991, it has been proven to be a safe, reliable, and effective method for CBD stones and has gained widespread acceptance with its additional advantage of being a single-stage approach [3]. Recent meta-analyses have found LCBDE to be superior to a two-stage approach (ERCP before or after LC) with regards to the total length of hospital stay, CBD stone clearance rate, and medical costs [6]. Additionally, LCBDE has the advantages of preserving the function of the sphincter of Oddi (SO), with lower morbidity and fewer ERCP-related complications [7, 8]. However, a history of prior abdominal operations posed a significant challenge for LCBDE because of the surgically altered gastrointestinal anatomy and adhesions [9].

Nevertheless, with the development of laparoscopic techniques and technological advances in equipment, a growing number of reports have suggested that laparoscopic procedures can also be performed as a standard treatment in patients with a history of abdominal operations [10, 11]. However, there are very few reports about laparoscopic procedures in patients with a history of abdominal biliary tract surgery. Thus, the objective of this study was to assess the effectiveness of LCBDE and evaluate the factors affecting the degree of postoperative adhesion in patients with previous abdominal biliary tract surgery. In the present study, we assessed the feasibility, safety, and influencing factors of postoperative adhesion of LCBDE in patients with CBD stones after abdominal biliary tract surgery and compared these factors with those of open surgery.

Methods

Patients and grou**

A total of 227 consecutive patients with CBD stones after abdominal biliary tract surgery who underwent surgical treatment at Zhongshan Hospital, Fudan University between December 2013 and June 2019 were retrospectively analyzed. Patients were grouped according to the surgical options: those who underwent LCBDE (n = 110) and those who underwent OCBDE (n = 117).

The diagnosis of CBD stones was based on conventional imaging tests, such as routine abdominal ultrasound, magnetic resonance cholangiopancreatography (MRCP) and relevant laboratory tests, including a routine blood examination, liver function tests (LFTs), and blood coagulation function tests. Medical clinical data were reviewed retrospectively, and the operative outcomes (including operative time, estimated blood loss, remnant CBD stones, open conversion, and postoperative hospital stay) and postoperative complications (including pulmonary diseases, bile leakage, wound infection, and postoperative bleeding) were collected and analyzed. The study protocol was approved by the institutional ethical committees of Zhongshan Hospital.

Definitions

Postoperative adhesions were divided into four classes according to the Operative Laparoscopy Study Group (OLSG) classification and adhesion scoring system proposed by Luciano et al. as follows: 0—no adhesions; 1—filmy, avascular adhesions and easily separable; 2—dense and/or vascular adhesions; and 3—cohesive adhesions [12, 13]. A wound infection involves only the skin or subcutaneous tissue and requires the documentation of one or more of the following: purulent drainage from the wound, aseptically obtained wound culture with isolated organisms, opening of the wound by a physician with clinical symptoms of infection, or diagnosis by a physician [14]. Postoperative pulmonary complications in our study mainly included pleural effusion, atelectasis and pneumonia. Hypertension and diabetes mellitus were diagnosed and confirmed by a specialist on the basis of clinical diagnostic criteria. Cardiovascular disease in our study mainly included coronary artery diseases, cardiomyopathy, abnormal heart rhythms, and myocardial ischemia. Pulmonary disease in our study mainly included asthma, chronic obstructive pulmonary disease, pulmonary fibrosis and pneumonia. Liver disease in our study mainly included viral hepatitis and cirrhosis. Cerebral diseases in our study mainly included cerebral infarction, cerebral thrombosis and cerebral hemorrhage.

Inclusion and exclusion criteria

The inclusion criteria were as follows: (1) a diagnosis of CBD stones confirmed by ultrasound, computerized tomography or MRCP before surgery, (2) patients who were not suitable for ERCP (e.g., those with stone relevant factors (multiple, large, impacted, and hilar stones), those with anatomic changes from the duodenal papilla, those who underwent some kind of gastrointestinal surgery, and those who could not tolerate or cooperate with or were hypersensitive to iodinated contrast media), (3) patients who failed ERCP in our institution or failed cannulation or those with incomplete stone clearance, and (4) patients with a history of at least one abdominal biliary tract surgery including LCBDE and OCBDE.

The exclusion criteria were as follows: (1) patients who did not have a history of abdominal biliary surgery and (2) patients who had contraindications for laparoscopic or open surgery.

Surgical procedure

All the procedures (including laparotomy and laparoscopic surgery) were performed by an experienced surgeon.

LCBDE technique

Patients in the LCBDE group were placed in a reverse Trendelenburg position under general anesthesia. We tended to use a three-trocar method: the first 10 mm trocar was placed in the subumbilical area for carbon dioxide insufflation and a 30° angled laparoscope. The second 10 mm trocar was located in the area below the xiphoid. The 5 mm and third trocar was placed in the midclavicular line, 1–2 cm under the right costal margin. Sometimes, an additional 5 mm trocar in the right anterior axillary line was needed when the adhesion was serious in the operation area. Cholecystectomy was performed first unless the patient had previously undergone the procedure. Careful dissection was used to identify the CBD, where a choledochotomy was performed with an approximately 1–1.5 cm longitudinal incision on the anterior surface. Then, a 5 mm flexible choledochoscope was regularly applied to find and remove stones with a stone basket, saline flushing, or electrohydraulic lithotripsy.

After clearance of the stones, a choledochoscope was used to confirm whether stones remained in the intrahepatic duct and CBD. If there was no residual stone, the choledochotomy incision was closed with a Vicryl 4–0 interrupted suture. For patients with a residual stone, a latex T-tube was placed at the operating surgeon’s discretion according to the condition of the CBD, which was then sewn with the same suture. A T-tube cholangiogram was performed 2–4 weeks postoperatively for patients who had T-tube drainage, and the T-tube was removed if there was no residual stone in the biliary system. For patients with a history of abdominal biliary tract surgery, the site of the first trocar was often chosen far from the original surgical site.

Open surgery technique

Patients in the open surgery group were placed in a reverse Trendelenburg position under general anesthesia, and the surgery was performed via a right upper quadrant subcostal incision. First, abdominal adhesions were separated carefully with blunt/sharp dissection, electrocautery or a harmonic scalpel. Cholecystectomy was performed first unless the patient had previously undergone the procedure. The CBD was dissected, and a choledochotomy was performed with an approximately 1.5 cm longitudinal incision on the anterior surface of the CBD. Last, the choledochoscope was regularly applied, and a T-tube was placed if necessary.

Postoperative treatment and follow-up

The patients were encouraged to be up and about as early as possible in the early stages after the surgery, and anticoagulant therapy could begin 24 h after surgery for patients at a high risk of thrombosis. Routine blood and blood biochemical examinations were performed every 72 h. An abdominal ultrasound was performed during the postoperative monitoring of fluid accumulation in the operative area for patients if necessary. If the patient had a cough, fever, or suspicious pleural effusion, chest computerized tomography was performed. If an abdominal cavity drainage tube was placed during the operation, it was removed when the drainage had stopped or became less than approximately 25 mL/day. If a T-tube was placed during the operation, it could be lifted up or clamped approximately one week after the patient was discharged. Outpatient follow-up was recommended for all patients 4 weeks after surgery, every 2 months for a minimum of 6 months, and imaging studies such as ultrasound or computed tomography were performed if there were problems. No patient was lost to follow-up.

Statistics

Classification variables are expressed as absolute numbers and percentages, while continuous variables are expressed as medians and ranges. Data analysis was performed using SPSS 20.0 (IBM, USA). Classification variables were analyzed between groups using the chi-square test or Fisher’s exact test, as appropriate. Continuous variables were analyzed between groups using the t test. The Cochran–Armitage test for trend was used in the categorical data analysis, which was performed with SAS 9.13 (Statistical Analysis System, USA). p < 0.05 was considered statistically significant.

Results

Patient characteristics

Between December 2013 and June 2019, a total of 227 patients who met the inclusion criteria were included in this study. A total of 110 patients underwent LCBDE, and 117 patients underwent OCBDE. Demographic details and relevant preoperative examination results are shown in Table 1. The results showed no obvious differences in terms of comorbidities such as hypertension, cardiovascular disease, pulmonary disease, liver disease, or cerebral diseases between the two groups, but there were more patients with diabetes mellitus in the LCBDE group than in the OCBDE group (p = 0.017). Moreover, both groups had similar histories of biliary surgery and American Society of Anesthesiologists (ASA) scores (p = 0.796 and p = 1.557, respectively). In addition, there were no obvious differences regarding the CBD size between the two groups (p = 0.705). However, there was a significant difference in the preoperative LFTs between the LCBDE group and the OCBDE group.

Table 1 Demographics and preoperative data of 227 patients included in the current study
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Operative outcomes and postoperative recovery

The operative outcomes are presented in Table 2. There was no significant difference in terms of the mean operation time between the LCBDE group and the OCBDE group (p = 0.067). The LCBDE group performed better than the OCBDE group with respect to estimated blood loss, remnant CBD stones, postoperative hospital stay and time to oral intake, with significant differences between the two groups (p = 0.041, p = 0.050, p = 0.041, and p = 0.015, respectively). A total of 19 patients (17%) in the LCBDE group were converted to open surgery. The reasons for open conversion were extensive intra-abdominal adhesions or severe fibrosis at the porta hepatis in 14 patients, incisional hernia near the original incision in 2 patients, a large number of bile duct stones around the hepatic hilar region in 1 patient, impacted stones in the left intrahepatic bile duct in 1 patient, and serious cirrhosis with varicose vessels on the surface of the CBD in 1 patient. With respect to postoperative complications, pulmonary diseases such as pneumonia and pleural effusion seemed to be the most common complications, affecting up to 32% and 42% of the LCBDE and OCBDE groups, respectively. In addition, bile leakage was the second most common postoperative complication, affecting 6% and 10% of the LCBDE and OCBDE groups, respectively. The patients with bile leakage recovered through symptomatic and supportive treatment, such as local drainage and anti-infective therapy. Empiric antibiotic treatment was first given for patients with infection, and the antibiotics were sometimes adjusted according to bacterial culture and drug sensitivity tests, especially for patients with severe infections. Moreover, wound infection was the third most common postoperative complication, affecting 3% and 3% of the LCBDE and OCBDE groups, respectively. The patients with wound infections recovered through wound dressing and local drainage. Finally, postoperative bleeding was found only in 3 patients. Exploratory laparotomy and digital subtraction angiography were applied to 1 patient in the LCBDE group, and the hemorrhage was ultimately found in a branch of the superior pancreaticoduodenal artery, which was treated by means of intravascular embolization. Digital subtraction angiography was applied to 1 patient in the OCBDE group, and the hemorrhage was ultimately found in a branch of the left hepatic artery, which was treated by means of intravascular embolization. An exploratory laparotomy was applied to another patient in the OCBDE group, and the hemorrhage was found in the gallbladder bed. Most importantly, there were no obvious differences in terms of the prevalence of pulmonary diseases (p = 0.117), bile leakage (p = 0.102), wound infection (p = 1.000), or postoperative bleeding (p = 1.000) between the two groups. There was no mortality in either group at the end of follow-up.

Table 2 Comparison of operative outcomes between groups
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Clavien’s classification of complications

According to Clavien’s classification of complications, Clavien grades II and IV were observed only in the OCBDE group, and Clavien grade V was not observed in either group. Clavien’s classification of complications is shown in Table 3. First, the postoperative course was normal (Clavien grade I) in most patients, and Clavien grade I accounted for 34% of the LCBDE group and 39% of the OCBDE group. Second, Clavien grade II complications in the OCBDE group included pleural effusion in 2 patients, bile leakage in 2 patients, and gastroparesis in 1 patient. Third, there were 3 and 6 Clavien grade III complications in the LCBDE and OCBDE groups, respectively. In the LCBDE group, 1 patient with intra-abdominal bleeding received exploratory laparotomy and digital subtraction angiography as mentioned above; 1 patient with postoperative intra-abdominal infection received ultrasound-guided drainage of abdominal fluid and anti-infective treatment; 1 patient with postoperative arytenoid dislocation received postoperative restoration treatment. In the OCBDE group, 2 patients with intra-abdominal bleeding received exploratory laparotomy and digital subtraction angiography separately, as mentioned above. Two patients with bile leakage and another 2 patients with pleural effusion recovered through ultrasound-guided local drainage. Finally, one patient with Clavien grade IV complications in the OCBDE group was diagnosed with acute renal failure after surgery and recovered after a series of treatments, including hemodialysis, anti-inflammatory drugs, and fluid replacement. Statistically significant differences in complications were discovered between the two groups (p = 0.045).

Table 3 Clavien’s classification of complications
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Factors affecting the degree of postoperative adhesion

Adhesions in the abdomen were seen mainly between the gallbladder liver bed and the neighboring organs (omentum, duodenum, right colon, and small bowel loops) or between the abdominal wall peritoneum [15]. Adhesions were divided into four classes according to the OLSG classification and adhesion scoring system proposed by Luciano et al. [12, 13, 15, 16]. The operation video was viewed by two operators and two reviewers. They independently scored each postoperative adhesion according to the OLSG classification. The overall adhesion score was 185 in the LCBDE group and 201 in the OCBDE group, and there was no significant difference between the two groups (p = 0.563). We further analyzed the factors affecting the degree of postoperative adhesion, which are shown in Table 4. In most patients, the postoperative adhesions were not serious; classes zero and 1, and class 2 accounted for 44% and 40% of all patients, respectively, while class 3 accounted for only 16% of all patients. There was no significant difference in sex, age, time of biliary disease (the duration of biliary disease from onset to admission), or time interval (the time interval between the first operation and the most recent operation) among classes zero and 1, 2 and 3 (p > 0.05). There was a significant difference in the previous number of operations, previous surgical approach and previous operation scope among classes zero and 1, 2 and 3 (p ≤ 0.05). After further comparison between groups with respect to the previous operation scope, we found a significant difference between previous gallbladder surgery and previous bile duct surgery and previous gallbladder surgery and previous gallbladder + bile duct surgery between classes zero and 1, 2 and 3 (p = 0.000 and p = 0.000, respectively). However, there was no significant difference between previous bile duct surgery and previous gallbladder + bile duct surgery between classes zero and 1, 2 and 3 (p = 0.245). Therefore, the above results demonstrated that multiple previous operations (≥ 2 times), a history of open surgery, and previous biliary tract surgery (including bile duct or gallbladder + bile duct other than cholecystectomy alone) were risk factors for postoperative adhesion.

Table 4 Factors affecting the degree of postoperative adhesion
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Discussion

In recent decades, with the development of new laparoscopic techniques and devices, LC has been recognized as the gold standard for the surgical management of gallstone diseases [17]. At the same time, the treatment for CBD stones has changed, and an increasing number of options are now prevalent. These new options include ERCP, endoscopic papillary balloon dilation (EPBD), or EST (if necessary) followed by LC; LC and intraoperative transcystic or direct CBD exploration; postoperative ERCP with EPBD/EST and stone extraction; intraoperative ERCP, EPBD/EST, and stone extraction during LC; and conversion to laparotomy [18, 19]. Therefore, there are two main surgical strategies in clinical practice: a single-stage surgical strategy involving LCBDE and stone retrieval at the time of LC and an alternative option of staged procedures, with LC and ERCP on separate dates for CBD stone clearance [20].

The advantage of staged procedures is the significantly shorter surgical time, but patients are exposed to the risks associated with ERCP, such as infection, pancreatitis, hemorrhage, and perforation. In addition, delays between the two stages of treatment may result in prolonged hospital admission [20, 21]. Furthermore, both endoscopic papillary large balloon dilation (EPLBD) alone and EST + EPLBD tend to result in a persistent and comparable loss of SO function, which is a likely cause of duodenobiliary reflux, bacterial contamination of the biliary tract, and subsequent late adverse events, including stone recurrence, cholangitis, or liver abscess [22]. Finally, the greatest concern following EST is the likelihood of develo** subsequent cholangiocarcinoma, and a number of authors have suggested that we be prudent to avoid a sphincterotomy in the very young until further studies clarify the situation in these patients [23]. Although both procedures are equivalent in terms of clinical outcomes, the single-stage surgical strategy can preserve the function of the SO, which effectively eliminates the potential serious risks of ERCP-associated complications and the need for further procedures [20, 24]. Moreover, the single-stage surgical strategy has a similar or better stone clearance rate, and it may be an ideal method for patients who fail ERCP because of difficult choledocholithiasis [25]. The single-stage surgical strategy has also been found to be safe and efficacious even in elderly patients [

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Funding

This work was supported by grants from The most important clinical medical center and key discipline construction of Shanghai (2017ZZ02007), National Natural Science Foundation of China (81600630 and 81872352), The Foundation of Shanghai Science and Technology Committee (16411952000), Clinical Study of Zhongshan Hospital (2018ZSLC24), JianFeng project of Xuhui Provincial Commission of Health and Family Planning (SHXH201703).

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  1. Min Li, Ying Tao, and Sheng Shen have contributed equally to this work.

Authors and Affiliations

  1. Department of General Surgery, Zhongshan Hospital, Fudan University, 180, Fenglin Road, Shanghai, 200032, China

    Min Li, Ying Tao, Sheng Shen, Lujun Song, Tao Suo, Han Liu, Yueqi Wang & Houbao Liu

  2. Department of General Surgery, Xuhui Central Hospital, Shanghai, 200031, China

    Dexiang Zhang & **aoling Ni

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  1. Min Li
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Dr. Min Li, Dr. Ying Tao, Dr. Sheng Shen, Dr. Lujun Song, Dr. Tao Suo, Dr. Han Liu, Dr. Yueqi Wang, Dr. Dexiang Zhang, Dr. **aoling Ni, Dr. Houbao Liu have no conflicts of interest or finical ties to disclosure.

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Li, M., Tao, Y., Shen, S. et al. Laparoscopic common bile duct exploration in patients with previous abdominal biliary tract operations. Surg Endosc 34, 1551–1560 (2020). https://doi.org/10.1007/s00464-020-07429-3

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