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Role of endoscopic retrograde cholangiopancreatography for suspected choledocholithiasis in patients undergoing laparoscopic cholecystectomy
Role of endoscopic retrograde cholangiopancreatography for suspected choledocholithiasis in patients undergoing laparoscopic cholecystectomy T. C. K. Tham, MD, MRCP, D. R. Lichtenstein, MD, J. Vandervoort, MD, R. C. K. Wong, MBBS, BSc D. Brooks, MD, J. Van Dam, MD, PhD, FACP, FACG, F. Ruymann, MD, F. Farraye, MD, FACP, FACG D. L. Carr-Locke, MD, FRCP, FACG Boston, Massachusetts
Background: We report our experience of selective cholangiography in a series of laparoscopic cholecystectomies and evaluate the strategy of using “stricter criteria” to select preoperative endoscopic retrograde cholangiopancreatography (ERCPs). Methods: A total of 1847 consecutive laparoscopic cholecystectomies were analyzed for use of cholangiography. A high risk of common bile duct stones (bilirubin level more than 2 mg/dL, jaundice, alkaline phosphatase level more than 150 U/L, pancreatitis, or dilated bile duct and/or stone on ultrasound or CT) was an indication for preoperative ERCP. Selective intraoperative cholangiography was performed for intermediate risk of bile duct stones. The strategy of using “stricter criteria” (jaundice and/or demonstrated bile duct stones on ultrasound or CT) for selecting preoperative ERCP was evaluated retrospectively. Results: Preoperative ERCP was performed in 135 patients (7.3%) and demonstrated bile duct stones in 43 (32%). Of 36 patients with mild gallstone pancreatitis alone, stones were found only in 6 patients (17%). Selective intraoperative cholangiography was performed in 87 (5%), and stones were found in 2 (2%); 67 (3.6%) postoperative ERCPs were performed for suspected choledocholithiasis, and stones were found in 21 (32%). Applying “stricter criteria” to select preoperative ERCP would predict ductal stones in 56%, whereas 3% of patients with stones would be missed, resulting in a 50% reduction in preoperative ERCPs. Conclusions: Even in selected patients considered likely to have choledocholithiasis, the diagnostic yield of preoperative ERCP is low. Using “stricter criteria” to select patients for preoperative ERCP can avoid unnecessary ERCPs. (Gastrointest Endosc 1998;47:50-6.)
Received June 21, 1996. For revision September 26, 1996. Accepted September 15, 1997. From the Division of Gastroenterology and Gastrointestinal Surgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts. Presented, in part, at the Annual Meeting of the American Society for Gastrointestinal Endoscopy, May 19-22, 1996, San Francisco, California (Gastrointest Endosc 1996;43:399). Reprint requests: Tony C. K. Tham, MD, MRCP, Consultant Gastroenterologist, Ulster Hospital, Dundonald, Belfast, BT16 0RH, Northern Ireland, United Kingdom. Copyright © 1998 by the American Society for Gastrointestinal Endoscopy 0016-5107/98/$5.00 1 0 37/1/86211 50 GASTROINTESTINAL ENDOSCOPY
Laparoscopic cholecystectomy has replaced open cholecystectomy as the procedure of choice in the vast majority of individuals with symptomatic cholelithiasis. The advantages of the laparoscopic technique include reduced pain, early discharge from hospital, rapid return to normal activity, and improved cosmetic appearance.1 As a result, both patients and physicians want to maintain the minimally invasive nature of the laparoscopic procedure and this has resulted in an expanded role for endoscopic retrograde cholangiopancreatography (ERCP) and endoscopic sphincterotomy for common bile duct stone removal. VOLUME 47, NO. 1, 1998
Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
T Tham, D Lichtenstein, J Vandervoort, et al.
Figure 1. Numbers of patients undergoing laparoscopic cholecystectomy who had preoperative ERCP, intraoperative cholangiography, and postoperative ERCP. Shaded areas indicate the cases analyzed for the “stricter criteria” strategy to select preoperative ERCP.
The optimal clinical strategy for using ERCP with laparoscopic cholecystectomy is unknown. When ERCP is performed before laparoscopic cholecystectomy in patients with suspected bile duct stones, the detection rate is low (27% to 50%).2-8 A decision analysis of the various approaches using ERCP in patients undergoing laparoscopic cholecystectomy concluded that postoperative ERCP resulted in the lowest cost, least procedure numbers, and least days lost from work.9 If the preoperative certainty of common bile duct stones approaches 100%, such as a visualized stone on ultrasound or CT, then preoperative ERCP would be essentially equivalent to postoperative ERCP.9 There has therefore been a move toward fewer preoperative and more postoperative ERCP except in patients who are jaundiced or who have bile duct stones as seen on ultrasound scan or CT.10 However no study to date has evaluated the strategy of selecting patients for preoperative ERCP on the basis of these stricter criteria. We report our experience of selective preoperative ERCP and intraoperative cholangiography (IOC) in the management of common bile duct stones in one of the largest series of laparoscopic cholecystectomies from a single center. We also assessed the accuracy of using stricter criteria (jaundice or common bile duct stones demonstrated on scan) for selecting preoperative ERCP. METHODS A total of 1847 consecutive laparoscopic cholecystectomies performed in this institution from 1990 through 1995 were analyzed for use of ERCP and IOC. A high risk of common duct stones was considered an indication for preoperative ERCP and was defined as a bilirubin level of more than 2 mg/dL (normal range 0.2 to 1.2 mg/dL), an VOLUME 47, NO. 1, 1998
alkaline phosphatase (ALK) level of more than 150 U/L (normal range 36 to 118 U/L), jaundice or pancreatitis (either present or recent), or dilated bile duct (diameter larger than 7 mm) or ductal stone on ultrasound or CT. Selective IOC was performed for intermediate risk based on either bilirubin 1.5 to 2 mg/dL, ALK 110 to 150 U/L, ALT/AST greater than twice upper limit of normal (normal range 7 to 52 and 9 to 30 U/L for ALT and AST, respectively), or remote history of jaundice/pancreatitis. Postoperative ERCP was performed in patients with suspected retained stones or bile duct injury. ERCP was performed with Fujinon ED7-XU2 and 310XU videoduodenoscopes. Biliary sphincterotomy was performed in a standard manner with the use of a variety of papillotomes (Microvasive, Boston, Mass.; Wilson-Cook, Winston-Salem, N.C.). Stones were extracted with retrieval balloons or dormia baskets after mechanical lithotripsy when necessary. The severity of pancreatitis before ERCP or cholecystectomy was decided by the attending physician on the basis of established criteria.11, 12 PostERCP complications were defined and classified according to published criteria.13 To analyze the strategy of using stricter criteria to select preoperative ERCPs, we reviewed the last 1097 laparoscopic cholecystectomies performed for ERCP involvement (Fig. 1). The initial 750 patients were not analyzed because there was insufficient data to indicate whether jaundice was persistent. The stricter criteria were defined as the presence of jaundice at the time of ERCP and/or demonstrated bile duct stones on noninvasive imaging.
RESULTS The proportion of common bile duct stones (i.e., number of patients with stones detected at preoperative or postoperative ERCP or IOC) was 4% (70 of 1847 cholecystectomies). ERCP was performed in 208 of 1847 cases (11%). GASTROINTESTINAL ENDOSCOPY 51
T Tham, D Lichtenstein, J Vandervoort, et al.
Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
Preoperative ERCP Preoperative ERCP was performed in 135 patients (7.3% of total cholecystectomies) and was successful in 133 (98.5%) (Fig. 1). Eight other patients who underwent preoperative ERCP did not fulfill the criteria for high likelihood of stones and were therefore excluded from the study. Bile duct stones were demonstrated in 43 patients (32% of preoperative ERCPs selected on the basis of a high likelihood of stones). None of the patients who did not fulfill the “high likelihood” criteria were found to have stones. All stones were successfully extracted after sphincterotomy in 42 and through an intact papilla in one patient. Other ERCP findings were as follows: bile crystals in two (1.4% of preoperative ERCP), common bile duct stricture in one (0.7%), pancreatic duct stricture in one (0.7%), Mirizzi’s syndrome in one (0.7%), and aberrant anatomy in two (1.4%). The remaining 83 ERCPs (62%) were normal. Thirty-six patients had mild gallstone pancreatitis alone. Stones were found in only six (17%) of these patients. In two other patients who were being investigated for recurrent pancreatitis with no gallstones on noninvasive imaging, the absence of stones was confirmed at surgery (pathology showed chronic cholecystitis but no stones) and bile crystals were found at ERCP. Intraoperative cholangiography Eighty-seven intraoperative cholangiograms (5% of cholecystectomies) were performed for “intermediate likelihood” of bile duct stones (Fig. 1). An additional 16 patients underwent IOC to determine the anatomy because the dissection was technically difficult. Bile duct stones were found in two (2% of those with suspected stones). One patient (1.1%) had a mildly dilated bile duct but no stones. The remaining 82 intraoperative cholangiograms (94%) were normal. Postoperative ERCP Postoperative ERCP was performed in 65 patients (3.5% of total cholecystectomies) (Fig. 1). ERCP was successful in 64 patients (98.5%). The unsuccessful ERCP was in a patient with a Billroth II partial gastrectomy. Bile leaks were found in 21 patients (33%), stones in 21 patients (33%), papillary stenosis in 3 (4.7%), and pancreatic duct stricture in 1 (1.6%). Thus the proportion of retained ductal stones in this series of laparoscopic cholecystectomies was 1.1%. The remaining 18 ERCPs (28%) were normal. The remaining 21 patients who had retained bile duct stones underwent successful endoscopic sphincterotomy and stone extraction. Their presenting 52 GASTROINTESTINAL ENDOSCOPY
features included abdominal pain in 78%, abnormal liver function tests in 44%, and pancreatitis in 22%; two patients had bile leaks. In 3 of the 21 patients, preoperative ERCP had been performed because they fulfilled the criteria for a high likelihood of ductal stones: one had a bile duct stone extracted, followed by a cholecystectomy 2 days later; in the other two patients, preoperative ERCP was normal and was followed by a cholecystectomy 1 week and 31⁄2 weeks later, respectively. A fourth patient did not undergo preoperative ERCP even though his ALK level was greater than 150 U/L. Seventeen patients (the remainder of the 21 patients who had retained bile duct stones) had no preoperative risk factors for common bile duct stones. Thus, the proportion of ductal stones found postoperatively in patients with no risk factors for ductal stones was 17 of (1847 2 135 2 87) or 1% (Fig. 1). The proportion of recurrent ductal stones after sphincterotomy and stone extraction is [1/43 (the number who underwent preoperative sphincterotomy and stone extraction)] 5 2% (95% CI [0, 7]). Complications Of all ERCPs undertaken, pancreatitis occurred in 9 of 208 patients (4.5%), hemorrhage in two (1%), and fever in one (0.5%). All patients recovered with conservative treatment. There was no mortality. In the 135 patients who underwent preoperative ERCP, pancreatitis occurred in six patients (4.1%); this followed a diagnostic procedure in five (three had mild and two had moderate pancreatitis) and a sphincterotomy plus stone extraction in one (moderate pancreatitis). Hemorrhage occurred in two patients (1.4%) after sphincterotomy; one was of mild and the other of moderate severity. One patient had a fever (0.7%) after a sphincterotomy and stone extraction, but blood cultures were negative. In the 65 patients who underwent postoperative ERCP, pancreatitis occurred in three patients (4.7%). It occurred after a sphincterotomy for a cystic duct leak in one patient (mild pancreatitis) and in two patients after stent insertion for bile leaks (one moderate and one severe pancreatitis). Stricter criteria for preoperative ERCP selection The last 1097 laparoscopic cholecystectomies were analyzed for the strategy of using “stricter criteria” for preoperative ERCP selection (Fig. 1, Table 1). Preoperative ERCP was performed in 107 cases (9.8%) with “high likelihood” of bile duct stones. In 34 cases (32%), stones were detected. ERCP failed in 1 (1%), but the subsequent IOC showed that there were no ductal stones. The findings at IOC and postoperative ERCP are shown in Table 1. VOLUME 47, NO. 1, 1998
Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
Table 1. ERCP and intraoperative cholangiograms among last 1097 patients undergoing laparoscopic cholecystectomy Procedure
Findings
Preoperative ERCT Stones Bile crystals CBD stricture PD stricture Normal Failed ERCP Intraoperative cholangiogram Mild dilated CBD Normal Postoperative ERCP Bile leaks Stones Ductal injury PD stricture Unsuccessful ERCP Normal Total ERCP involvement
CBD, Common bile duct; PD, pancreatic duct. *Subsequent intraoperative cholangiogram showed there were no stones in the bile duct.
If the strategy of using “stricter criteria” in these 1097 patients was applied, it would be predicted that only 54 of the patients (5%) would have undergone preoperative ERCP (Table 2). This would result in a predicted 50% reduction in the number of patients selected for preoperative ERCP. In these patients, stones would have been found in 30 patients. The proportion of finding bile duct stones preoperatively using “stricter criteria” would have increased from an actual 32% (34 of 107) to a predicted 56% (30 of 54). Four patients with stones would have been missed preoperatively but would then have undergone IOC according to the strategy. Thus, if the “stricter criteria” had been applied, the proportion of patients with bile duct stones missed preoperatively would be predicted to be 3% of all patients with bile duct stones suspected preoperatively (4 of 149). Of the 1097 patients, bile duct stones were found in nine patients at ERCP postoperatively and none were found on IOC. In the nine patients with ductal stones found at postoperative ERCP, there was no clinical suspicion of ductal stones before the cholecystectomy. There were therefore no false negative preoperative ERCPs. DISCUSSION Although there are other reports of ERCP in patients undergoing laparoscopic cholecystectomy,2-8 VOLUME 47, NO. 1, 1998
Table 2. ERCP findings if “stricter criteria” were used to select preoperative ERCPs
No. (%) 107 (9.8) 34 (32) 1 (0.9) 1 (0.9) 1 (0.9) 69 (64) 1 (0.9)* 42 (3.6) 1 (2) 41 (98) 40 (3.6) 14 (35) 9 (22) 1 (2.5) 2 (5) 1 (2.5) 13 (32) 147 (13.4)
T Tham, D Lichtenstein, J Vandervoort, et al.
Bile duct stones found Bile duct stones not found Total
Preoperative ERCP indicated according to “stricter criteria”
Preoperative ERCP not indicated according to “stricter criteria”
Total
30
4
34
24
49
73
54
53
107
All these 107 patients underwent preoperative ERCP as selected by the criteria for “high likelihood” of bile duct stones.
ours has the largest number of patients from a single center. Even in patients considered likely to have bile duct stones, we found that the positive diagnostic yield of preoperative ERCP was low (32%). This is supported by the results of other studies in which the diagnostic yield ranged from 25% to 50%.2-8 The 7% of our laparoscopic cholecystectomy patients who fulfilled the criteria for preoperative ERCP is similar to that of other published reports2-8, 10 and approaches 10%. With adoption of this policy, about 30,000 ERCPs with negative results would be performed annually in the United States in the 600,000 patients scheduled for laparascopic cholecystectomy.10 Thus there is a need to refine the selection criteria for preoperative ERCP to avoid unnecessary investigations and to reduce risk and costs. Mild gallstone pancreatitis was associated with a low incidence of bile duct stones (17%), as has been noted in other studies.14-16 Thus prior gallstone pancreatitis is a poor indication for preoperative ERCP. By contrast, there is a higher rate of positive findings with postoperative ERCP after selective IOC (72%). The incidence of retained stones after cholecystectomy in our series was low at 1.1% presumably because of, in part, prior patient selection for preoperative ERCP and IOC. However, in patients presenting postoperatively with abdominal pain and abnormal liver function tests, there is a high chance of a positive ERCP finding such as a retained stone or bile leak. Three patients had ductal stones on postoperative ERCP despite having had preoperative ERCP (one with ductal stone and two normal). Explanations for this include the following: passage of a stone from the gallbladder into the duct in the time interval between preoperative ERCP and cholecystectomy (which ranged from 1 to 31⁄2 weeks), transfer of a GASTROINTESTINAL ENDOSCOPY 53
T Tham, D Lichtenstein, J Vandervoort, et al.
Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
Figure 2. Proposed algorithm for the role of ERCP in patients undergoing laparoscopic cholecystectomies. *Bilirubin 1.5 to 2 mg/dL, alkaline phosphatase more than 110 U/L, past jaundice, ALT/AST greater than twice normal, pancreatitis (mild, present, or past), dilated bile duct on scan. **Patients who did not fulfill any of the above criteria. ES, Endoscopic sphincterotomy; CBDE, common bile duct exploration.
stone into the duct during manipulation of the gallbladder at surgery, or ductal stones could have been missed or the duct incompletely cleared preoperatively. To refine the selection criteria for preoperative ERCP so as to avoid unnecessary investigations, costs, and hospital stay, we evaluated the strategy of using “stricter criteria” (jaundice and/or ductal stones seen on imaging) for ERCP. The number of preoperative ERCPs could be reduced by half while the proportion of ductal stones found doubled. The caveat is that stones will be missed in a small number of patients, but these should be detected with IOC and can be removed postoperatively by ERCP. Laparoscopic IOC has been found to be accurate for the diagnosis of bile duct stones with a false-positive rate of 4% and false-negative rate of 5%9 and is successful in 91%.17 The preliminary results of a randomized trial, which compared preoperative ERCP with selective postoperative ERCP in patients found to have stones by IOC or with symptoms of retained stones, found that the latter strategy is associated with a shorter hospital stay.18 Thus there is a tendency toward performing fewer preoperative ERCPs but more IOC followed if necessary by selective postoperative ERCP. As far as we are aware, only our study and that of Stevens et al.18 have specifically evaluated this change in practice in 54 GASTROINTESTINAL ENDOSCOPY
patients. The results of a formal decision analysis of the different approaches to the use of ERCP in patients undergoing laparoscopic cholecystectomy supports our findings.9 This showed that postoperative ERCP minimized costs and morbidity; however, when a ductal stone is likely (e.g., stones seen on scan), then selective preoperative ERCP may be a clinically equivalent strategy.9 Based on our results and those of other studies, we suggest an algorithm for the management of bile duct stones (Fig. 2). Any strategy must be modified according to local expertise and experience which may permit reliance on IOC and postoperative ERCP, whereas the lack of expertise in these areas favor preoperative ERCP and open exploration. Preoperative ERCP has the advantage that open bile duct exploration can still be performed if all stones cannot be successfully removed. On the other hand, postoperative ERCP has the advantage of limiting the number of negative preoperative studies when combined with IOC. There has already been a gradual move away from preoperative ERCP in centers where expertise is available to remove stones reliably in the postoperative period. A decision analysis suggests that preoperative ERCP followed by open exploration if necessary would be favored if ERCP had less than 75% diagnostic and less than 50% therapeutic success rates or lengthened hospitalizaVOLUME 47, NO. 1, 1998
Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
tion by more than 7 days.9 After preoperative ERCP, regardless of whether ductal stones are found, we believe that cholecystectomy should be performed as soon as possible to avoid passage of gallstones into the common bile duct in the interim. We also assume that most centers at present do not perform laparoscopic common bile duct exploration as the techniques for this procedure are still evolving and are performed reliably in only few medical centers.19-21 Laparoscopic duct exploration has the advantage of a one-stage procedure for the patient found to have ductal stones at surgery. Preliminary prospective randomized trials of singlestage laparoscopic bile duct exploration and laparoscopic cholecystectomy versus combined ERCP and laparoscopic cholecystectomy suggest that the single-stage laparoscopic technique is just as effective as ERCP in clearing the duct of stones, has a similar morbidity, but is associated with a significantly shorter hospital stay.22, 23 In terms of cost, combined ERCP and laparoscopic cholecystectomy is likely to be more expensive than laparoscopic common bile duct exploration with cholecystectomy because of the reduction in hospital stay with the latter approach24 and differences in total professional fees. The use of this technique is likely to increase in the future.10 Should it become routinely available in most centers, the algorithm for the management of bile duct stones is likely to change. Intraoperative ERCP has also been described25 but is logistically cumbersome. Ideally the choices among the various treatment options should be based on direct prospective comparisons that determine total costs, complication rates, as well as treatment efficacy. Outcome trials comparing the various clinical strategies for ERCP have not been performed, owing to the large numbers of patients required for comparison and the variability in technical expertise for these procedures among institutions. In conclusion, despite performing preoperative ERCP on the basis of accepted criteria for a high likelihood of bile duct stones, the incidence of stones is low. It may be possible to modify the indications for ERCP to avoid unnecessary procedures, decrease morbidity, and reduce costs. The strategy of selecting patients for preoperative ERCP based on a high likelihood of bile duct stones (jaundice or ductal stones seen on ultrasound or CT) and subjecting the remaining patients suspected of ductal stones to IOC followed by postoperative ERCP if indicated, appears to be reasonable. Further prospective studies would be required to confirm this recommendation. If laparoscopic common bile duct exploration becomes VOLUME 47, NO. 1, 1998
T Tham, D Lichtenstein, J Vandervoort, et al.
more widely available, this may become the procedure of choice for ductal stones with a consequent decline in the number of ERCPs. REFERENCES 1. McMahon AJ, Russel IT, Baxter JN, Ross R, Anderson JR, Morran CG, et al. Laparoscopic versus mini laparotomy cholecystectomy: a randomized controlled trial. Lancet 1994; 343:135-8. 2. Graham SM, Flowers JL, Scott TR, Bailey RW, Scovill WA, Zucker KA, et al. Laparoscopic cholecystectomy and common bile duct stones. The utility of planned perioperative endoscopic retrograde cholangiography and sphincterotomy: experience with 63 patients. Ann Surg 1993;218:61-7. 3. Sauerbruch T. Endoscopic management of bile duct stones. J Gastroenterol Hepatol 1992;7:328-34. 4. Arregui ME, Davis CJ, Arkush A, Nagan RF. Laparoscopic cholecystectomy combined with endoscopic sphincterotomy and stone extraction or laparoscopic choledochoscopy and electrohydraulic lithotripsy for management of cholelithiasis and choledocholithiasis. Surg Endosc 1992;58:206-10. 5. Baird DR, Wilson JP, Mason EM, Duncan TD, Evans JS, Luke JP, et al. An early review of 800 laparoscopic cholecystectomies at a university affiliated community teaching hospital. Am Surg 1992;58:206-10. 6. Graves HA Jr, Ballinger JF, Anderson WJ. Appraisal of laparoscopic cholecystectomy. Ann Surg 1991;213:655-64. 7. Larson GM, Vitale GC, Casey J, Evons JS, Gillam G, Heuser L, et al. Multipractice analysis of laparoscopic cholecystectomy in 1983 patients. Am J Surg 1992;163:221-6. 8. Tham TCK, Collins JSA, Watson RGP, Ellis PK, McIlrath EM. Diagnosis of common bile duct stones by intravenous cholangiography and their prediction by ultrasound and liver function tests compared to endoscopic retrograde cholangiography. Gastrointest Endosc 1996;44:158-63. 9. Erickson RA, Carlson B. The role of endoscopic retrograde cholangiopancreatography in patients with laparoscopic cholecystectomies. Gastroenterology 1995;109:252-63. 10. Strasberg SM, Soper NJ. Management of choledocholithiasis in the laparoscopic era. Gastroenterology 1995;109:320-2. 11. Agarwal N, Pitchumoni CS. Assessment of severity in acute pancreatitis. Am J Gastroenterol 1991;86:1385. 12. Banks PA. Predictors of severity in acute pancreatitis. Pancreas 1991;6(Suppl 1):S7-12. 13. Cotton PB, Lehman G, Vennes J, Geenen JE, Russell RCG, Meyers WC, et al. Endoscopic sphincterotomy complications and their management: an attempt at consensus. Gastrointest Endosc 1991;37:383-93. 14. Tate JJT, Lau WY, Li AKC. Laparoscopic cholecystectomy for biliary pancreatitis. Br J Surg 1994;81:720-2. 15. Rhodes M, Armstrong CP, Longstaff A, Cawthorn S. Laparoscopic cholecystectomy with endoscopic retrograde cholangiopancreatography for acute gallstone pancreatitis. Br J Surg 1993;80:247. 16. Soper NJ, Brunt LM, Callery MP, Edmunodowicz SA, Aliperti G. Role of laparoscopic cholecystectomy in the management of acute gallstone pancreatitis. Am J Surg 1994;167:4251. 17. Flowers JL, Zucker KA, Graham SM, Scovill WA, Imbembo AL, Bailey RW. Laparoscopic cholangiography. Results and indications. Ann Surg 1992;215:209-16. 18. Stevens PD, Van de Mierop F, Green PHR, Chabot JA, Stein JA, Garcia-Carrasquillo RJ, et al. ERCP before or after laparoscopic cholecystectomy? Final results from a randomized trial: length of stay differences [abstract]. Gastroenterology 1996:110:A477. 19. Carroll BJ, Fallas MJ, Phillips EH. Laparoscopic transcystic choledochoscopy. Surg Endosc 1994;8:310-4. 20. Hunter JG. Laparoscopic cholecystectomy and the common bile duct. Surg Endosc 1994;8:285-6. GASTROINTESTINAL ENDOSCOPY 55
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21. Binmoeller KF, Soehendra N, Liguory C. The common bile duct stone: Time to leave it to the laparoscopic surgeon? Endoscopy 1994;26:315-9. 22. Rhodes M, Sussman L. Prospective randomized trial of laparoscopic common bile duct exploration versus post-operative ERCP [abstract]. Gut 1997;40(Suppl 1):A68. 23. Cuschieri A, the EAES Ductal Stone Group. EAES ductal stone study—preliminary findings of multi-centre prospec-
tive randomized trial comparing two-stage versus single stage management [abstract]. Gut 1996;39(Suppl 1):A43. 24. Fletcher DR. Laparoscopic cholecystectomy in Australia— outcomes and costs. Surg Endosc 1995;9:1230-5. 25. Deslandres E, Gagner M, Pomp A, Rheault M, Ledu R, Clermont R, et al. Intraoperative endoscopic sphincterotomy for common bile duct stones during laparoscopic cholecystectomy. Gastrointest Endosc 1993;39:54-8.
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56 GASTROINTESTINAL ENDOSCOPY
VOLUME 47, NO. 1, 1998
Background: We report our experience of selective cholangiography in a series of laparoscopic cholecystectomies and evaluate the strategy of using “stricter criteria” to select preoperative endoscopic retrograde cholangiopancreatography (ERCPs). Methods: A total of 1847 consecutive laparoscopic cholecystectomies were analyzed for use of cholangiography. A high risk of common bile duct stones (bilirubin level more than 2 mg/dL, jaundice, alkaline phosphatase level more than 150 U/L, pancreatitis, or dilated bile duct and/or stone on ultrasound or CT) was an indication for preoperative ERCP. Selective intraoperative cholangiography was performed for intermediate risk of bile duct stones. The strategy of using “stricter criteria” (jaundice and/or demonstrated bile duct stones on ultrasound or CT) for selecting preoperative ERCP was evaluated retrospectively. Results: Preoperative ERCP was performed in 135 patients (7.3%) and demonstrated bile duct stones in 43 (32%). Of 36 patients with mild gallstone pancreatitis alone, stones were found only in 6 patients (17%). Selective intraoperative cholangiography was performed in 87 (5%), and stones were found in 2 (2%); 67 (3.6%) postoperative ERCPs were performed for suspected choledocholithiasis, and stones were found in 21 (32%). Applying “stricter criteria” to select preoperative ERCP would predict ductal stones in 56%, whereas 3% of patients with stones would be missed, resulting in a 50% reduction in preoperative ERCPs. Conclusions: Even in selected patients considered likely to have choledocholithiasis, the diagnostic yield of preoperative ERCP is low. Using “stricter criteria” to select patients for preoperative ERCP can avoid unnecessary ERCPs. (Gastrointest Endosc 1998;47:50-6.)
Received June 21, 1996. For revision September 26, 1996. Accepted September 15, 1997. From the Division of Gastroenterology and Gastrointestinal Surgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts. Presented, in part, at the Annual Meeting of the American Society for Gastrointestinal Endoscopy, May 19-22, 1996, San Francisco, California (Gastrointest Endosc 1996;43:399). Reprint requests: Tony C. K. Tham, MD, MRCP, Consultant Gastroenterologist, Ulster Hospital, Dundonald, Belfast, BT16 0RH, Northern Ireland, United Kingdom. Copyright © 1998 by the American Society for Gastrointestinal Endoscopy 0016-5107/98/$5.00 1 0 37/1/86211 50 GASTROINTESTINAL ENDOSCOPY
Laparoscopic cholecystectomy has replaced open cholecystectomy as the procedure of choice in the vast majority of individuals with symptomatic cholelithiasis. The advantages of the laparoscopic technique include reduced pain, early discharge from hospital, rapid return to normal activity, and improved cosmetic appearance.1 As a result, both patients and physicians want to maintain the minimally invasive nature of the laparoscopic procedure and this has resulted in an expanded role for endoscopic retrograde cholangiopancreatography (ERCP) and endoscopic sphincterotomy for common bile duct stone removal. VOLUME 47, NO. 1, 1998
Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
T Tham, D Lichtenstein, J Vandervoort, et al.
Figure 1. Numbers of patients undergoing laparoscopic cholecystectomy who had preoperative ERCP, intraoperative cholangiography, and postoperative ERCP. Shaded areas indicate the cases analyzed for the “stricter criteria” strategy to select preoperative ERCP.
The optimal clinical strategy for using ERCP with laparoscopic cholecystectomy is unknown. When ERCP is performed before laparoscopic cholecystectomy in patients with suspected bile duct stones, the detection rate is low (27% to 50%).2-8 A decision analysis of the various approaches using ERCP in patients undergoing laparoscopic cholecystectomy concluded that postoperative ERCP resulted in the lowest cost, least procedure numbers, and least days lost from work.9 If the preoperative certainty of common bile duct stones approaches 100%, such as a visualized stone on ultrasound or CT, then preoperative ERCP would be essentially equivalent to postoperative ERCP.9 There has therefore been a move toward fewer preoperative and more postoperative ERCP except in patients who are jaundiced or who have bile duct stones as seen on ultrasound scan or CT.10 However no study to date has evaluated the strategy of selecting patients for preoperative ERCP on the basis of these stricter criteria. We report our experience of selective preoperative ERCP and intraoperative cholangiography (IOC) in the management of common bile duct stones in one of the largest series of laparoscopic cholecystectomies from a single center. We also assessed the accuracy of using stricter criteria (jaundice or common bile duct stones demonstrated on scan) for selecting preoperative ERCP. METHODS A total of 1847 consecutive laparoscopic cholecystectomies performed in this institution from 1990 through 1995 were analyzed for use of ERCP and IOC. A high risk of common duct stones was considered an indication for preoperative ERCP and was defined as a bilirubin level of more than 2 mg/dL (normal range 0.2 to 1.2 mg/dL), an VOLUME 47, NO. 1, 1998
alkaline phosphatase (ALK) level of more than 150 U/L (normal range 36 to 118 U/L), jaundice or pancreatitis (either present or recent), or dilated bile duct (diameter larger than 7 mm) or ductal stone on ultrasound or CT. Selective IOC was performed for intermediate risk based on either bilirubin 1.5 to 2 mg/dL, ALK 110 to 150 U/L, ALT/AST greater than twice upper limit of normal (normal range 7 to 52 and 9 to 30 U/L for ALT and AST, respectively), or remote history of jaundice/pancreatitis. Postoperative ERCP was performed in patients with suspected retained stones or bile duct injury. ERCP was performed with Fujinon ED7-XU2 and 310XU videoduodenoscopes. Biliary sphincterotomy was performed in a standard manner with the use of a variety of papillotomes (Microvasive, Boston, Mass.; Wilson-Cook, Winston-Salem, N.C.). Stones were extracted with retrieval balloons or dormia baskets after mechanical lithotripsy when necessary. The severity of pancreatitis before ERCP or cholecystectomy was decided by the attending physician on the basis of established criteria.11, 12 PostERCP complications were defined and classified according to published criteria.13 To analyze the strategy of using stricter criteria to select preoperative ERCPs, we reviewed the last 1097 laparoscopic cholecystectomies performed for ERCP involvement (Fig. 1). The initial 750 patients were not analyzed because there was insufficient data to indicate whether jaundice was persistent. The stricter criteria were defined as the presence of jaundice at the time of ERCP and/or demonstrated bile duct stones on noninvasive imaging.
RESULTS The proportion of common bile duct stones (i.e., number of patients with stones detected at preoperative or postoperative ERCP or IOC) was 4% (70 of 1847 cholecystectomies). ERCP was performed in 208 of 1847 cases (11%). GASTROINTESTINAL ENDOSCOPY 51
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Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
Preoperative ERCP Preoperative ERCP was performed in 135 patients (7.3% of total cholecystectomies) and was successful in 133 (98.5%) (Fig. 1). Eight other patients who underwent preoperative ERCP did not fulfill the criteria for high likelihood of stones and were therefore excluded from the study. Bile duct stones were demonstrated in 43 patients (32% of preoperative ERCPs selected on the basis of a high likelihood of stones). None of the patients who did not fulfill the “high likelihood” criteria were found to have stones. All stones were successfully extracted after sphincterotomy in 42 and through an intact papilla in one patient. Other ERCP findings were as follows: bile crystals in two (1.4% of preoperative ERCP), common bile duct stricture in one (0.7%), pancreatic duct stricture in one (0.7%), Mirizzi’s syndrome in one (0.7%), and aberrant anatomy in two (1.4%). The remaining 83 ERCPs (62%) were normal. Thirty-six patients had mild gallstone pancreatitis alone. Stones were found in only six (17%) of these patients. In two other patients who were being investigated for recurrent pancreatitis with no gallstones on noninvasive imaging, the absence of stones was confirmed at surgery (pathology showed chronic cholecystitis but no stones) and bile crystals were found at ERCP. Intraoperative cholangiography Eighty-seven intraoperative cholangiograms (5% of cholecystectomies) were performed for “intermediate likelihood” of bile duct stones (Fig. 1). An additional 16 patients underwent IOC to determine the anatomy because the dissection was technically difficult. Bile duct stones were found in two (2% of those with suspected stones). One patient (1.1%) had a mildly dilated bile duct but no stones. The remaining 82 intraoperative cholangiograms (94%) were normal. Postoperative ERCP Postoperative ERCP was performed in 65 patients (3.5% of total cholecystectomies) (Fig. 1). ERCP was successful in 64 patients (98.5%). The unsuccessful ERCP was in a patient with a Billroth II partial gastrectomy. Bile leaks were found in 21 patients (33%), stones in 21 patients (33%), papillary stenosis in 3 (4.7%), and pancreatic duct stricture in 1 (1.6%). Thus the proportion of retained ductal stones in this series of laparoscopic cholecystectomies was 1.1%. The remaining 18 ERCPs (28%) were normal. The remaining 21 patients who had retained bile duct stones underwent successful endoscopic sphincterotomy and stone extraction. Their presenting 52 GASTROINTESTINAL ENDOSCOPY
features included abdominal pain in 78%, abnormal liver function tests in 44%, and pancreatitis in 22%; two patients had bile leaks. In 3 of the 21 patients, preoperative ERCP had been performed because they fulfilled the criteria for a high likelihood of ductal stones: one had a bile duct stone extracted, followed by a cholecystectomy 2 days later; in the other two patients, preoperative ERCP was normal and was followed by a cholecystectomy 1 week and 31⁄2 weeks later, respectively. A fourth patient did not undergo preoperative ERCP even though his ALK level was greater than 150 U/L. Seventeen patients (the remainder of the 21 patients who had retained bile duct stones) had no preoperative risk factors for common bile duct stones. Thus, the proportion of ductal stones found postoperatively in patients with no risk factors for ductal stones was 17 of (1847 2 135 2 87) or 1% (Fig. 1). The proportion of recurrent ductal stones after sphincterotomy and stone extraction is [1/43 (the number who underwent preoperative sphincterotomy and stone extraction)] 5 2% (95% CI [0, 7]). Complications Of all ERCPs undertaken, pancreatitis occurred in 9 of 208 patients (4.5%), hemorrhage in two (1%), and fever in one (0.5%). All patients recovered with conservative treatment. There was no mortality. In the 135 patients who underwent preoperative ERCP, pancreatitis occurred in six patients (4.1%); this followed a diagnostic procedure in five (three had mild and two had moderate pancreatitis) and a sphincterotomy plus stone extraction in one (moderate pancreatitis). Hemorrhage occurred in two patients (1.4%) after sphincterotomy; one was of mild and the other of moderate severity. One patient had a fever (0.7%) after a sphincterotomy and stone extraction, but blood cultures were negative. In the 65 patients who underwent postoperative ERCP, pancreatitis occurred in three patients (4.7%). It occurred after a sphincterotomy for a cystic duct leak in one patient (mild pancreatitis) and in two patients after stent insertion for bile leaks (one moderate and one severe pancreatitis). Stricter criteria for preoperative ERCP selection The last 1097 laparoscopic cholecystectomies were analyzed for the strategy of using “stricter criteria” for preoperative ERCP selection (Fig. 1, Table 1). Preoperative ERCP was performed in 107 cases (9.8%) with “high likelihood” of bile duct stones. In 34 cases (32%), stones were detected. ERCP failed in 1 (1%), but the subsequent IOC showed that there were no ductal stones. The findings at IOC and postoperative ERCP are shown in Table 1. VOLUME 47, NO. 1, 1998
Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
Table 1. ERCP and intraoperative cholangiograms among last 1097 patients undergoing laparoscopic cholecystectomy Procedure
Findings
Preoperative ERCT Stones Bile crystals CBD stricture PD stricture Normal Failed ERCP Intraoperative cholangiogram Mild dilated CBD Normal Postoperative ERCP Bile leaks Stones Ductal injury PD stricture Unsuccessful ERCP Normal Total ERCP involvement
CBD, Common bile duct; PD, pancreatic duct. *Subsequent intraoperative cholangiogram showed there were no stones in the bile duct.
If the strategy of using “stricter criteria” in these 1097 patients was applied, it would be predicted that only 54 of the patients (5%) would have undergone preoperative ERCP (Table 2). This would result in a predicted 50% reduction in the number of patients selected for preoperative ERCP. In these patients, stones would have been found in 30 patients. The proportion of finding bile duct stones preoperatively using “stricter criteria” would have increased from an actual 32% (34 of 107) to a predicted 56% (30 of 54). Four patients with stones would have been missed preoperatively but would then have undergone IOC according to the strategy. Thus, if the “stricter criteria” had been applied, the proportion of patients with bile duct stones missed preoperatively would be predicted to be 3% of all patients with bile duct stones suspected preoperatively (4 of 149). Of the 1097 patients, bile duct stones were found in nine patients at ERCP postoperatively and none were found on IOC. In the nine patients with ductal stones found at postoperative ERCP, there was no clinical suspicion of ductal stones before the cholecystectomy. There were therefore no false negative preoperative ERCPs. DISCUSSION Although there are other reports of ERCP in patients undergoing laparoscopic cholecystectomy,2-8 VOLUME 47, NO. 1, 1998
Table 2. ERCP findings if “stricter criteria” were used to select preoperative ERCPs
No. (%) 107 (9.8) 34 (32) 1 (0.9) 1 (0.9) 1 (0.9) 69 (64) 1 (0.9)* 42 (3.6) 1 (2) 41 (98) 40 (3.6) 14 (35) 9 (22) 1 (2.5) 2 (5) 1 (2.5) 13 (32) 147 (13.4)
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Bile duct stones found Bile duct stones not found Total
Preoperative ERCP indicated according to “stricter criteria”
Preoperative ERCP not indicated according to “stricter criteria”
Total
30
4
34
24
49
73
54
53
107
All these 107 patients underwent preoperative ERCP as selected by the criteria for “high likelihood” of bile duct stones.
ours has the largest number of patients from a single center. Even in patients considered likely to have bile duct stones, we found that the positive diagnostic yield of preoperative ERCP was low (32%). This is supported by the results of other studies in which the diagnostic yield ranged from 25% to 50%.2-8 The 7% of our laparoscopic cholecystectomy patients who fulfilled the criteria for preoperative ERCP is similar to that of other published reports2-8, 10 and approaches 10%. With adoption of this policy, about 30,000 ERCPs with negative results would be performed annually in the United States in the 600,000 patients scheduled for laparascopic cholecystectomy.10 Thus there is a need to refine the selection criteria for preoperative ERCP to avoid unnecessary investigations and to reduce risk and costs. Mild gallstone pancreatitis was associated with a low incidence of bile duct stones (17%), as has been noted in other studies.14-16 Thus prior gallstone pancreatitis is a poor indication for preoperative ERCP. By contrast, there is a higher rate of positive findings with postoperative ERCP after selective IOC (72%). The incidence of retained stones after cholecystectomy in our series was low at 1.1% presumably because of, in part, prior patient selection for preoperative ERCP and IOC. However, in patients presenting postoperatively with abdominal pain and abnormal liver function tests, there is a high chance of a positive ERCP finding such as a retained stone or bile leak. Three patients had ductal stones on postoperative ERCP despite having had preoperative ERCP (one with ductal stone and two normal). Explanations for this include the following: passage of a stone from the gallbladder into the duct in the time interval between preoperative ERCP and cholecystectomy (which ranged from 1 to 31⁄2 weeks), transfer of a GASTROINTESTINAL ENDOSCOPY 53
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Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
Figure 2. Proposed algorithm for the role of ERCP in patients undergoing laparoscopic cholecystectomies. *Bilirubin 1.5 to 2 mg/dL, alkaline phosphatase more than 110 U/L, past jaundice, ALT/AST greater than twice normal, pancreatitis (mild, present, or past), dilated bile duct on scan. **Patients who did not fulfill any of the above criteria. ES, Endoscopic sphincterotomy; CBDE, common bile duct exploration.
stone into the duct during manipulation of the gallbladder at surgery, or ductal stones could have been missed or the duct incompletely cleared preoperatively. To refine the selection criteria for preoperative ERCP so as to avoid unnecessary investigations, costs, and hospital stay, we evaluated the strategy of using “stricter criteria” (jaundice and/or ductal stones seen on imaging) for ERCP. The number of preoperative ERCPs could be reduced by half while the proportion of ductal stones found doubled. The caveat is that stones will be missed in a small number of patients, but these should be detected with IOC and can be removed postoperatively by ERCP. Laparoscopic IOC has been found to be accurate for the diagnosis of bile duct stones with a false-positive rate of 4% and false-negative rate of 5%9 and is successful in 91%.17 The preliminary results of a randomized trial, which compared preoperative ERCP with selective postoperative ERCP in patients found to have stones by IOC or with symptoms of retained stones, found that the latter strategy is associated with a shorter hospital stay.18 Thus there is a tendency toward performing fewer preoperative ERCPs but more IOC followed if necessary by selective postoperative ERCP. As far as we are aware, only our study and that of Stevens et al.18 have specifically evaluated this change in practice in 54 GASTROINTESTINAL ENDOSCOPY
patients. The results of a formal decision analysis of the different approaches to the use of ERCP in patients undergoing laparoscopic cholecystectomy supports our findings.9 This showed that postoperative ERCP minimized costs and morbidity; however, when a ductal stone is likely (e.g., stones seen on scan), then selective preoperative ERCP may be a clinically equivalent strategy.9 Based on our results and those of other studies, we suggest an algorithm for the management of bile duct stones (Fig. 2). Any strategy must be modified according to local expertise and experience which may permit reliance on IOC and postoperative ERCP, whereas the lack of expertise in these areas favor preoperative ERCP and open exploration. Preoperative ERCP has the advantage that open bile duct exploration can still be performed if all stones cannot be successfully removed. On the other hand, postoperative ERCP has the advantage of limiting the number of negative preoperative studies when combined with IOC. There has already been a gradual move away from preoperative ERCP in centers where expertise is available to remove stones reliably in the postoperative period. A decision analysis suggests that preoperative ERCP followed by open exploration if necessary would be favored if ERCP had less than 75% diagnostic and less than 50% therapeutic success rates or lengthened hospitalizaVOLUME 47, NO. 1, 1998
Role of ERCP for suspected choledocholithiasis with laparoscopic cholecystectomy
tion by more than 7 days.9 After preoperative ERCP, regardless of whether ductal stones are found, we believe that cholecystectomy should be performed as soon as possible to avoid passage of gallstones into the common bile duct in the interim. We also assume that most centers at present do not perform laparoscopic common bile duct exploration as the techniques for this procedure are still evolving and are performed reliably in only few medical centers.19-21 Laparoscopic duct exploration has the advantage of a one-stage procedure for the patient found to have ductal stones at surgery. Preliminary prospective randomized trials of singlestage laparoscopic bile duct exploration and laparoscopic cholecystectomy versus combined ERCP and laparoscopic cholecystectomy suggest that the single-stage laparoscopic technique is just as effective as ERCP in clearing the duct of stones, has a similar morbidity, but is associated with a significantly shorter hospital stay.22, 23 In terms of cost, combined ERCP and laparoscopic cholecystectomy is likely to be more expensive than laparoscopic common bile duct exploration with cholecystectomy because of the reduction in hospital stay with the latter approach24 and differences in total professional fees. The use of this technique is likely to increase in the future.10 Should it become routinely available in most centers, the algorithm for the management of bile duct stones is likely to change. Intraoperative ERCP has also been described25 but is logistically cumbersome. Ideally the choices among the various treatment options should be based on direct prospective comparisons that determine total costs, complication rates, as well as treatment efficacy. Outcome trials comparing the various clinical strategies for ERCP have not been performed, owing to the large numbers of patients required for comparison and the variability in technical expertise for these procedures among institutions. In conclusion, despite performing preoperative ERCP on the basis of accepted criteria for a high likelihood of bile duct stones, the incidence of stones is low. It may be possible to modify the indications for ERCP to avoid unnecessary procedures, decrease morbidity, and reduce costs. The strategy of selecting patients for preoperative ERCP based on a high likelihood of bile duct stones (jaundice or ductal stones seen on ultrasound or CT) and subjecting the remaining patients suspected of ductal stones to IOC followed by postoperative ERCP if indicated, appears to be reasonable. Further prospective studies would be required to confirm this recommendation. If laparoscopic common bile duct exploration becomes VOLUME 47, NO. 1, 1998
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more widely available, this may become the procedure of choice for ductal stones with a consequent decline in the number of ERCPs. REFERENCES 1. McMahon AJ, Russel IT, Baxter JN, Ross R, Anderson JR, Morran CG, et al. Laparoscopic versus mini laparotomy cholecystectomy: a randomized controlled trial. Lancet 1994; 343:135-8. 2. Graham SM, Flowers JL, Scott TR, Bailey RW, Scovill WA, Zucker KA, et al. Laparoscopic cholecystectomy and common bile duct stones. The utility of planned perioperative endoscopic retrograde cholangiography and sphincterotomy: experience with 63 patients. Ann Surg 1993;218:61-7. 3. Sauerbruch T. Endoscopic management of bile duct stones. J Gastroenterol Hepatol 1992;7:328-34. 4. Arregui ME, Davis CJ, Arkush A, Nagan RF. Laparoscopic cholecystectomy combined with endoscopic sphincterotomy and stone extraction or laparoscopic choledochoscopy and electrohydraulic lithotripsy for management of cholelithiasis and choledocholithiasis. Surg Endosc 1992;58:206-10. 5. Baird DR, Wilson JP, Mason EM, Duncan TD, Evans JS, Luke JP, et al. An early review of 800 laparoscopic cholecystectomies at a university affiliated community teaching hospital. Am Surg 1992;58:206-10. 6. Graves HA Jr, Ballinger JF, Anderson WJ. Appraisal of laparoscopic cholecystectomy. Ann Surg 1991;213:655-64. 7. Larson GM, Vitale GC, Casey J, Evons JS, Gillam G, Heuser L, et al. Multipractice analysis of laparoscopic cholecystectomy in 1983 patients. Am J Surg 1992;163:221-6. 8. Tham TCK, Collins JSA, Watson RGP, Ellis PK, McIlrath EM. Diagnosis of common bile duct stones by intravenous cholangiography and their prediction by ultrasound and liver function tests compared to endoscopic retrograde cholangiography. Gastrointest Endosc 1996;44:158-63. 9. Erickson RA, Carlson B. The role of endoscopic retrograde cholangiopancreatography in patients with laparoscopic cholecystectomies. Gastroenterology 1995;109:252-63. 10. Strasberg SM, Soper NJ. Management of choledocholithiasis in the laparoscopic era. Gastroenterology 1995;109:320-2. 11. Agarwal N, Pitchumoni CS. Assessment of severity in acute pancreatitis. Am J Gastroenterol 1991;86:1385. 12. Banks PA. Predictors of severity in acute pancreatitis. Pancreas 1991;6(Suppl 1):S7-12. 13. Cotton PB, Lehman G, Vennes J, Geenen JE, Russell RCG, Meyers WC, et al. Endoscopic sphincterotomy complications and their management: an attempt at consensus. Gastrointest Endosc 1991;37:383-93. 14. Tate JJT, Lau WY, Li AKC. Laparoscopic cholecystectomy for biliary pancreatitis. Br J Surg 1994;81:720-2. 15. Rhodes M, Armstrong CP, Longstaff A, Cawthorn S. Laparoscopic cholecystectomy with endoscopic retrograde cholangiopancreatography for acute gallstone pancreatitis. Br J Surg 1993;80:247. 16. Soper NJ, Brunt LM, Callery MP, Edmunodowicz SA, Aliperti G. Role of laparoscopic cholecystectomy in the management of acute gallstone pancreatitis. Am J Surg 1994;167:4251. 17. Flowers JL, Zucker KA, Graham SM, Scovill WA, Imbembo AL, Bailey RW. Laparoscopic cholangiography. Results and indications. Ann Surg 1992;215:209-16. 18. Stevens PD, Van de Mierop F, Green PHR, Chabot JA, Stein JA, Garcia-Carrasquillo RJ, et al. ERCP before or after laparoscopic cholecystectomy? Final results from a randomized trial: length of stay differences [abstract]. Gastroenterology 1996:110:A477. 19. Carroll BJ, Fallas MJ, Phillips EH. Laparoscopic transcystic choledochoscopy. Surg Endosc 1994;8:310-4. 20. Hunter JG. Laparoscopic cholecystectomy and the common bile duct. Surg Endosc 1994;8:285-6. GASTROINTESTINAL ENDOSCOPY 55
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21. Binmoeller KF, Soehendra N, Liguory C. The common bile duct stone: Time to leave it to the laparoscopic surgeon? Endoscopy 1994;26:315-9. 22. Rhodes M, Sussman L. Prospective randomized trial of laparoscopic common bile duct exploration versus post-operative ERCP [abstract]. Gut 1997;40(Suppl 1):A68. 23. Cuschieri A, the EAES Ductal Stone Group. EAES ductal stone study—preliminary findings of multi-centre prospec-
tive randomized trial comparing two-stage versus single stage management [abstract]. Gut 1996;39(Suppl 1):A43. 24. Fletcher DR. Laparoscopic cholecystectomy in Australia— outcomes and costs. Surg Endosc 1995;9:1230-5. 25. Deslandres E, Gagner M, Pomp A, Rheault M, Ledu R, Clermont R, et al. Intraoperative endoscopic sphincterotomy for common bile duct stones during laparoscopic cholecystectomy. Gastrointest Endosc 1993;39:54-8.
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