Evaluation of perioperative cholangiography in one thousand laparoscopic cholecystectomies

Introduction
Laparoscopic cholecystectomy (LC) has gained acceptance as the gold standard for gallbladder removal; however, the roles of intraoperative cholangiography (IOCG) and perioperative endoscopic retrograde cholangiopancreatography (ERCP) are controversial. Because of the technical expertise required for both laparoscopic IOCG and common bile duct exploration, many authors have recommended preoperative ERCP in patients suspected of having common duct stones (1-4). This approach prevents unnecessary IOCG which may result in false negative studies and unnecessary open common bile duct explorations. Other authors recommend routine IOCG as a means of preventing missed common duct stones and avoiding intraoperative bile duct injuries (5-7).
Regardless of their recommendations for the timing and use of IOCG and ERCP, nearly all studies confirm that accurately defining patients with choledocholithiasis is difficult (8, 27). Ultimately, the surgeon chooses between unnecessary IOCG or ERCP studies. Though achieving it through different means, both approaches aim to prevent a second operative procedure to remove retained common duct stones. Selective use of IOCG with laparoscopic transcystic common bile duct (CBD) stone extraction or common bile duct exploration is well elaborated (9, 10) while laparoscopic fiberoscopy procedures are continuously evolving (11, 12).
In this study, we evaluated 1002 consecutive attempted laparoscopic cholecystectomies at Indiana University School of Medicine since the procedure was first performed in July of 1990. We reviewed the indications for and results of all IOCGs and ERCPs performed on patients undergoing laparoscopic cholecystectomy during a five and one-half year period in attempt to establish an algorithm for their effective use.

Methods
The records of 1002 consecutive patients undergoing attempted laparoscopic cholecystectomy between July of 1990 and December of 1995 at a university medical center were reviewed. The procedure was successfully completed in 941 patients and converted to an open procedure in 61 patients (6% conversion rate). Patients who underwent successful laparoscopic cholecystectomy were included in the study to evaluate the role of ERCP and IOCG.
The procedures were performed at Wishard Memorial Hospital, a county hospital (n=487), Indiana University Hospital, a private teaching hospital (n=471) and J. W. Riley Hospital for Children (n=44). All procedures were performed by second through fifth year general surgery residents, always under the supervision of one of ten staff general or pediatric surgeons. The procedures were performed as previously described by Reddick and Olsen (13), with particular emphasis on separating the neck of the gallbladder from the hepatic bed as recommended by Hunter (14). The Arrow TM cholangiocatheter kit was used for IOCG, which was performed with the aid of intraoperative real-time fluoroscopy and subtraction cholangiography. Parameters evaluated included indication for operation, history of jaundice, pancreatitis, previous upper or lower abdominal operations, serum biochemistry values, biliary radiological studies, and major complications.
Patients undergoing cholangiography were retrospectively divided into two groups. Patients with a history of jaundice or pancreatitis, abnormal alkaline phosphatase, SGOT, bilirubin, or amylase values, or radiological (imaging modalities) evidence of dilated extra- or intrahepatic bile ducts or choledocholithiasis were considered "at risk" for choledocholithiasis. Those without any of the above findings were deemed "unlikely" to have choledocholithiasis. Intraoperative cholangiography was attempted in 272 patients (28.9%) and successful in 234 (86%). Eighty-six patients (9.1%) underwent ERCP, 67 preoperatively and 19 postoperatively.

Results
One thousand and two laparoscopic cholecystectomies were reviewed for this study. The median age of adults was 40 with a range of 18-92, while the median age of pediatric patients was 10 with a range of 4-17. Indications for choleycstectomy are listed in Table 1. Sixty-one procedures required conversion to open procedures with reasons for conversion including unclear anatomy, bleeding, bowel injury, equipment failure, and most commonly inflammation or adhesions.
IOCG was attempted in 272 patients (28.9%) and completed in 234 (86%) (Table 2). Based on preoperative evaluation, 62 patients (26.5%) were considered "at risk" for choledocholithiasis while 172 patients (73.5%) were deemed "unlikely" to have stones. In the "unlikely" group, only 3 patients (1.7%) had intraoperative cholangiograms showing choledocholithiasis (Fig. 1). The duct was cleared laparoscopically in 2 patients and passed prior to ERCP in the third patient. In the "at risk" group, 21 cholangiograms (34%) showed choledocholithiasis of which 12 (57%) were successfully cleared laparoscopically (Fig. 2). Postoperative ERCP was performed in the other 9 patients with endoscopic clearance of the duct required in 6 cases (29%). The remaining ERCPs showed no pathological findings and were nontherapeutic.
Eighty six patients (9.1% of the patients undergoing successful laparoscopic chlolecystectomy) had ERCP in the perioperative period (Table 3). Sixty-four of the 67 patients (95.5%) undergoing preoperative ERCP were at risk for CBDS; however, choledocholithiasis was found in only 25 patients (39%). The remaining three patients did not have stones. Therefore, 22 of 64 preoperative ERCPs (34%) were therapeutic. On the other hand, 78.9% (15 of 19) of the postoperative ERCPs were therapeutic. Specifically, 12 of the 14 (86%) of the postoperative ERCPs "at risk" had stones, while 3 of 5 patients in the "unlikely" group had stones.

Discussion
The management of common duct stones and the use of IOCG and ERCP continues to generate much controversy. It begins with identifying those patients at risk for having retained stones. In the era of open cholecystectomy, surgeons at our institution practiced selective use of IOCG in patients with a dilated common bile duct, history of jaundice, cholangitis, or pancreatitis, and small stones in the gallbladder with a large cystic duct. Those patients with filling defects within the intra- or extrahepatic biliary tree or with obstruction of the flow of bile into the duodenum, as well as those with palpable stones in the duct, underwent common bile duct exploration. Preoperative ERCP was reserved for patients with cholangitis unresponsive to antibiotics or those suspected of having carcinoma. These criteria are very sensitive and miss only 1%-4% of unsuspected common bile duct stones in the entire cholecystectomy population (15, 16, 17). Our experience supports this sensitivity as only 3 of 172 (1.7%) patients deemed unlikely to have stones were found to have stones on routine IOCG.
The 1993 National Institute of Health consensus statement recommended preoperative ERCP or transhepatic cholangiography for all patients with clinical suspicion of common bile duct stones (18). Using liberal and sensitive criteria, this approach results in a high number of nontherapeutic ERCPs. Clair, in a prospective evaluation, performed preoperative ERCP in 25 patients deemed likely to have stones based on biochemical, radiological, or clinical evidence, and identified and extracted stones in 6 (24%) patients (2). Korman reported 27 (64%) therapeutic preoperative ERCPs in 42 patients suspected of having choledocholithiasis based on "surgeon's judgement" (4). In our experience, the operating surgeon obtained a preoperative ERCP in 64 patients with indications for cholangiography. The decision to obtain preoperative ERCP or perform IOCG was based on surgeon's preference, although these patients met clinical, biochemical, or radiological criteria. Twenty-five (39%) of these procedures necessitated endoscopic removal of choledocholithiasis. In these three and similar series, using liberal criteria for preoperative ERCP results in between 40% and 70% unnecessary studies, with their attendant risks and costs. Such an aggressive recommendation is not supported by our data.
Two other reports have used models of discriminant analysis to more accurately predict the presence of common bile duct stones. Trondsen et al. retrospectively evaluated age, bilirubin, AST, and GGT in 599 patients, and reported a false positive rate of 3.7% and a false negative rate of 1.8% (19). Barkun et al. also described a model which predicted a 94% probability of choledocholithiasis (20). These methods are promising means of predicting common bile duct stones preoperatively and may ultimately supplant traditional clinical parameters. At the present time, however, the models need further prospective evaluation and interinstitutional testing.
Because of the large number of nontherapeutic preoperative ERCPs, many surgeons have replaced preoperative cholangiography with IOCG. Surgeons, however, are unable to agree on when to perform IOCG. Generally, the opinion is divided between selective and routine cholangiography. Those who recommend routine cholangiography argue that IOCG identifies unsuspected stones and allows clearance in a one stage procedure (5-7, 21, 22). In addition, routine IOCG enables the operator to identify aberrant anatomy and may help to prevent or provide early recognition of bile duct injury. Those who recommend selective use of cholangiography argue that cholangiography is time consuming, expensive, and has a false positive rate of 2-4%. In addition, the incidence of common duct injuries is nearly equal regardless of whether or not IOCG is performed (23, 24, 25). However, IOCG during LC is the most cost-effective means of preventing delayed recognition of bile duct injuries (26). In a decision model incorporating cost ratios, test accuracy complication, and failure rates of 4 peri-laparoscopic strategies, Sahai et al. (27) found IOCG the least costly for their "intermediate-risk" patients (risk of stones 17-34%), ERCP for "high risk" patients (risk of stones higher than 55%) and if expert endoscopic ultrasound (EUS) available expectant management for "low risk" patients (risk of stones 0-10%). Cost-efficacy for laparoscopic cholecystectomy patients depends primarily on the risk of stones and stone-related symptoms, but procedural costs and operator expertise are also critical. A consensus has not yet been reached, and may be settled ultimately by cost issues.
Our data support the selective use of IOCG. Of the three patients with unsuspected stones noted on cholangio-graphy, two underwent successful laparoscopic transcystic common bile duct clearance (Fig. 3-4), while the third passed the stone spontaneously prior to ERCP. It is uncertain whether these stones were incidentally pushed from the gallbladder into the common duct during the cholecystecomy or whether they were present prior to operation. The asymptomatic nature of these stones, their small size, and relative ease of clearance may explain the apparent benign nature of the clinical course. In addition, three patients with no indication for cholangiography who did not undergo cholangiography returned in the early postoperative period with jaundice and required common duct clearance with ERCP. None of these patients presented with pancreatitis.
Using a selective philosophy for IOCG with traditional clinical and biochemical indicators of choledocholithiasis still produces a significant number of nontherapeutic studies. Only 34% (21/62) of the IOCGs performed on patients with suspicion of choledocholithiasis had choledocholithiasis in this series. Of the 21 patients with abnormal studies, 12 (57%) underwent successful laparoscopic clearance (Fig. 3-4), subjecting them to a single procedure. Six of the patients' ducts were effectively cleared by postoperative ERCP, while 3 had nontherapeutic postoperative ERCPs. Our nontherapeutic rates of preoperative ERCP and of IOCG are 34% and 39%, respectively, and no patients experienced complications as a result of IOCG attempts.
Diagnostic ERCP has a 1%-5% risk of pancreatitis and requires a second procedure for definitive treatment of cholelithiasis (28). Further, the incidence of pancreatitis is even greater following therapeutic ERCP (29). Although most patients experience mild amylase elevations and abdominal pain which resolve with supportive care, they do require additional hospitalization. Approximately 10% of patients with post-ERCP pancreatitis develop severe pancreatitis which requires surgical intervention (29). Stanten and Frey evaluated 24 patients during a 4 year period with clinically significant pancreatitis after ERCP (30). The average length of hospitalization for the entire group was 12.8 days and six patients eventually required surgical intervention. The overall mortality was 13% in this 24 patient population.
Despite positive findings on IOCG, no patients in this series were converted for the purpose of exploring the common bile duct. In this experience, postoperative ERCP was universally successful in clearing common ducts which could not be cleared laparoscopically, or when laparoscopic clearance was not attempted. Endoscopists successfully clear the duct over 90% of the time (24). The common bile ducts of patients with Bilroth II and Roux-en-y gastroenteric anastomoses are difficult to access endoscopically. In addition, patients with common duct stones larger than 1.5 cm or with multiple stones present a particular challenge to the endoscopist. None of our patients required a second operative procedure to address retained common duct stones, although the reliance on postoperative ERCP will likely lead to the need for operative exploration.

Figura 1

Figura 2

Figura 3

Figura 4

Conclusion
In summary, because of the inability of clinical and biochemical parameters to accurately predict choledocholithiasis, preoperative ERCPs are recommended only for patients with evidence of choledocholithiasis, cholangitis unresponsive to antibiotics, suspicion of carcinoma, and, possibly, gallstone pancreatitis which does not improve with supportive care. Intraoperative cholangiography is indicated selectively for patients with biochemical, radiological/ultrasound, or clinical suspicion of choledocholithiasis. Although IOCG leads to an equal percentage of nontherapeutic studies as preoperative ERCP, it generally allows definitive treatment with one procedure. Following an abnormal IOCG, attempts should be made to clear the duct laparoscopically. If these are unsuccessful, postoperative ERCP is indicated. Conversion to an open procedure for common bile duct exploration should be considered in patients with gastroenteric anastamoses, common duct stones larger than 1.5cm, and multiple common duct stones.

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