TECHNOLOGICAL REVIEW The elective evaluation of patients with suspected choledocholithiasis undergoing laparoscopic cholecystectomy Frances Tse, MD, Jeffrey S. Barkun, MD, CM, MSc (clinical epidemiology), Alan N. Barkun, MD, CM, MSc (clinical epidemiology) Montreal, Canada
Common bile duct (CBD) stones occur in 10% to 15% of patients with symptomatic gallstones undergoing cholecystectomy.1-3 In general, CBD stones should be removed, because they may be associated with severe complications, such as pancreatitis and cholangitis.4 There are many possible management approaches, depending on the preferred diagnostic and therapeutic modality: ERCP, intra-operative cholangiogram (IOC), EUS, MRCP, intra-operative US (IOUS), intravenous cholangiography (IVC), and helical CT cholangiography (hCTC). Controversy persists because of the variety of approaches, the difficulty of comparing all strategies in all-encompassing prospective trials, the regional variation in expertise and availability of technologies. The purpose of this article is to review competing technologies and approaches for diagnosing CBD stones with regard to diagnostic performance characteristics, technical success, safety, and costeffectiveness. Patients with symptomatic cholelithiasis in whom choledocholithiasis is suspected before cholecystectomy, based on clinical or laboratory clues, are the primary focus of this review. The specific management of patients with cholangitis, gallstone pancreatitis, and bile duct stones after cholecystectomy will not be addressed. An algorithm for the management of suspected CBD stones is put forward based on evidence and the quality thereof. Future areas for investigation of the different diagnostic modalities for the detection of CBD stones are proposed. Current affiliations: Divisions of Gastroenterology and General Surgery, Montreal General Hospital and Royal Victoria Hospital Sites, McGill University Health Centre, Montreal, Quebec. Reprint requests: Dr. Alan N. Barkun, Division of Gastroenterology, Montreal General Hospital Site, McGill University Health Centre, 1650 Cedar Ave., Rm. D7.148, Montreal, Quebec, Canada, H3G 1A4. Copyright Ó 2004 by the American Society for Gastrointestinal Endoscopy 0016-5107/$30.00 PII: S0016-5107(04)01457-9 VOLUME 60, NO. 3, 2004
REVIEW METHODOLOGY A systematic search was performed for relevant articles published in the English language by using MEDLINE, PubMed, and the Cochrane Controlled Trials Register from 1966 to December 2003. The search strategy included the key terms: choledocholithiasis, cholecystectomy, cholangiography, endoscopic, intravenous, laparoscopic, intra-operative, ultrasonography, magnetic resonance imaging, computed tomography, surgery, complications, decision support techniques, costs and cost analysis, costbenefit analysis, sensitivity and specificity, comparative study, and prospective studies. Information was collected on study design, prevalence of CBD stones, type of imaging modalities used for diagnosis and/or management of CBD stones, technical success, diagnostic performance characteristics, side effects, and costs. Sensitivity, specificity, and positive predictive value (PPV) and negative predictive value (NPV) were abstracted. The grading of recommendations in this manuscript is based on the grading put forth by Ball et al. (http:// www.cebm.net/levels_of_evidence.asp). In this grading system, the level of recommendation is supported by evidence that is based on: 1a, a systematic review of available RCTs; 1b, an individual RCT; 2a, a systematic review of available cohort studies; 2b, an individual cohort study; 2c, outcomes research or ecological studies; 3a, a systematic review of available case-control studies; 3b, an individual casecontrol study; 4, case-series; 5, expert opinion.5,6 CURRENT TECHNOLOGY ERCP ERCP traditionally has been considered the standard of reference for the diagnosis of CBD stones. Frey et al.7 noted that ERCP had a sensitivity of 90%, a specificity of 98%, and an accuracy of 96% in the evaluation of CBD stones when IOC was used as the reference. ERCP is successful in clearing CBD stones in 85% to 90% of cases when standard procedures, such as endoscopic sphincterotomy (ES) and balloon or basket stone extraction, are used.8-13 For those patients who fail standard techniques, mechanical lithotripsy will increase the success rate to more than 90%.14-15 A major benefit of ERCP in the evaluation of CBD stones is that ERCP provides a means of diagnosis and therapeutic intervention in the same setting. However, large prospective case series have found overall complication rates of 5% to 10% and mortality rates of 0.02% to 0.5% after diagnostic and therapeutic ERCP.16-19 The most common complication is acute pancreatitis, occurring in 5% of cases, GASTROINTESTINAL ENDOSCOPY
437
F Tse, J Barkun, A Barkun
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
Table 1. Prospective studies of IOC with n > 50 that provided data on the success rates, sensitivity, and specificity of IOC during laparoscopic cholecystectomy in the diagnosis of CBD stones Investigator Greig et al.105 Ohtani et al.31 Rothlin et al.25 Machi et al.28 Barteau et al.24 Tranter et al.104 Flowers et al.32 Stiegmann et al.106 Siperstein et al.33 Thompson et al.27 Birth et al.35 Catheline et al.26 Weighted averages*
Study type Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective,
non-random non-random non-random non-random non-random non-random non-random non-random non-random non-random non-random non-random
N
Success (%)
Sensitivity (%)
Specificity (%)
54 65 100 100 125 135 165 209 300 360 518 600
89% 83% 100% 92% 100% 90% 91% 93% 94% 98% 92% 83% 91%: 95% CI[90, 92]
83% 80% 75% 88% 93% 86% 100% 59% 96% 95% 100% 78% 87%: 95% CI[86, 88]
95% 97% 99% 98% 96% 99% 98% 100% 100% 100% 98% 97% 98%: 95% CI[97, 99]
PPV (%)
NPV (%)
71% 98% 100% 78% 76% 100% 98% 100% 100% 100% 82% 79% 89%: 95% CI[88, 90]
98% 95% 95% 98% 99% 98% 100% 95% 99% 99% 100% 98% 98%: 95% CI[97, 99]
IOC, Intra-operative cholangiogram; CBD, common bile duct; PPV, positive predictive value; NPV, negative predictive value; CI, confidence interval. *Weighted averages were based on the total number of patients (n = 2731); 95% CI were calculated by using the normal approximation of the binomial distribution.
and being moderate to severe in about 1%16-20 Because of its attendant risks and the availability of safer noninvasive cholangiographic methods with comparable diagnostic abilities, the sole use of diagnostic ERCP should, and likely will in most instances, become extinct.4 Certainly, the routine use of pre-operative ERCP, with a substantial rate of negative examinations and the risk of complications, is unacceptable.17-23 IOC Intra-operative cholangiography is considered, along with ERCP, to be the reference standard against which all other imaging modalities of the biliary tree are evaluated. Intra-operative cholangiography is performed during cholecystectomy by contrast injection through a catheter introduced into the cystic duct, with successful cannulation rates of greater than 90%.11,12,24-35 Overall, IOC has a sensitivity of 87%: 95% CI[86, 88] and a specificity of 98%: 95% CI[97, 99] in the detection of CBD stones (Table 1).24-35 The complication rate related to IOC is less than 0.1%.32,36 There exists a long-standing debate between the use of routine and selective IOC. Supporters of routine IOC claim this practice ensures fewer retained stones, fewer postoperative ERCPs, and a reduction in the number of CBD injuries.37-41 The main disadvantages of routine IOC are an increase in operating time and false-positive findings (2%).36,42,43 Arguably, the most convincing data in the open cholecystectomy (OC) or laparoscopic cholecystectomy (LC) era alike would favor the selective use of IOC (level 1A).36,44,45 With respect to the prevention 438
GASTROINTESTINAL ENDOSCOPY
of bile duct injuries, the routine use of IOC remains controversial.37,46,47 Percutaneous transhepatic cholangiography In the last decade, percutaneous transhepatic cholangiography has been primarily used as an alternative to surgery in patients with failed ERCP who require biliary drainage.22,48-51 This imaging modality will not be reviewed here, because it is not considered to be a routine initial diagnostic or therapeutic approach in patients with CBD stones. MRCP MRCP is performed with high-resolution breathhold T2-weighed sequences that depict the biliary tract as a bright structure without the use of contrast material or ionizing radiation.52-55 The high-signal intensity of the biliary tract makes it well suited for the detection of CBD stones. Current techniques permit imaging of the entire biliary tract in a single breathhold of 20 seconds or less and provide high spatial resolution so that structures such as 4th-order intrahepatic bile ducts and small stones are readily detected in many cases.56-58 A recent authoritative meta-analysis59 of 67 published controlled trials shows that MRCP has excellent overall sensitivity (95%: 95% CI[75, 99]) and specificity (97%: 95% CI [86, 99]) for demonstrating the level and the presence of biliary obstruction. However, MRCP is less sensitive for detecting stones (91%: 95% CI[73, 97]) or differentiating malignant from benign obstruction (88%: 95% CI[70, 96]). Moreover, the sensitivity for detecting stones seems to decrease according to stone size: 67% to 100% for VOLUME 60, NO. 3, 2004
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
F Tse, J Barkun, A Barkun
Table 2. Studies of EUS with n > 50 that provided data on the sensitivity, specificity, and accuracy of EUS in the diagnosis of CBD stones* Investigator Buscarini et al.74 Palazzo et al.75 Sugiyama et al.76 Kohut et al.77 Shim et al.78 Prat et al.79 Canto et al.80 Amouyal et al.72 Norton et al.81 Weighted averagesy
Study type
N
Prevalence (%)
Prospective, non-random Retrospective, non-random Prospective, non-random Prospective, non-random Prospective, non-random Prospective, non-random Prospective, non-random Prospective, non-random Prospective, non-random
485 422 142 134 132 119 64 62 50
59% 36% 36% 68% 21% 66% 30% 52% 48%
Sensitivity (%)
Specificity (%)
Accuracy (%)
98% 95% 96% 93% 89% 93% 84% 97% 88% 95%: 95% CI[94, 96]
99% 98% 100% 93% 100% 97% 95% 100% 96% 98%: 95% CI[97, 99]
97% 96% 99% 94% 97% 95% 94% 98% 92% 96%: 95% CI[95, 97]
CBD, Common bile duct; CI, confidence interval. *ERCP, percutaneous transhepatic cholangiography, laparoscopic CBD exploration, or open CBD exploration used as reference standards. yWeighted averages were based on the total number of patients (n = 1610); 95% CI were calculated by using the normal approximation of the binomial distribution.
stones greater than 10 mm in size, 89% to 94% for stones measuring 6 to 10 mm, and 33% to 71% for bile duct stones less than 6 mm in size.60-63 Overall, there is level 2A evidence that MRCP is accurate for the detection of CBD stones; however, its ability to diagnose small stones in non-dilated ducts may be limited. The major advantage of MRCP is the noninvasive nature of the procedure. It does not require exposure to radiation or to contrast agents. Diagnostic images can be obtained in the vast majority of patients, including those who have complex bilio-enteric anastomoses.64 As well, MRCP can demonstrate the biliary tree above and below a complete obstruction.53 The major disadvantages of MRCP compared with ERCP are lower spatial resolution,65 unit availability, lack of an immediate therapy that can be provided for duct obstruction, claustrophobia, and the inability to evaluate patients with pacemakers or ferromagnetic implants. Causes of possible artifact include pneumobilia, normal vessels, flow artifacts, and duodenal diverticulum.66-68 A stone impacted at the ampulla may be missed.69 As well, a low insertion of the cystic duct may be mistaken for a dilated CBD,70 and clips in the abdomen from previous surgery may distort images.71 EUS EUS involves the endoscopic insertion of an US probe into the stomach and the second stage of the duodenum, allowing for sonographic images of the CBD to be obtained without the interference of subcutaneous fat and bowel gas.72,73 By using high frequencies (7, 5, and 12 MHz), the resolution of EUS is less than 1 mm. A stone in the CBD appears as a hyperechoic focus with associated acoustic shadowing. EUS is extremely accurate in diagnosing VOLUME 60, NO. 3, 2004
CBD stones, with a sensitivity of 95%: 95% CI[94, 96]), specificity of 98%: 95% CI[97, 99], and an accuracy of 96%: 95% CI[95, 97].72-81 Table 2 summarizes the major studies that provided data on the sensitivity, the specificity, and the accuracy of EUS in the diagnosis of CBD stones. These results are far superior to US (sensitivity 63%) and CT (sensitivity 71%)76 and were approximately equivalent to that of ERCP. EUS is especially more sensitive than US or CT in detecting small stones and those stones that are situated within a small caliber CBD.76 Napoleon et al.82 followed, for at least 1 year, 328 patients undergoing EUS for suspicion of CBD stones; 230 had normal EUS findings, and the negative predictive value of EUS for the diagnosis of CBD stones was 95%. A recent prospective, controlled study suggested that EUS may be more accurate than MRCP for detecting CBD stones.83 EUS and MRCP were performed in 43 patients suspected of having CBD stones. The sensitivity of EUS was 100%, the specificity was 95%, the PPV was 91%, the NPV was 100%, and the overall accuracy was 97%. The corresponding values for MRCP were 100%, 73%, 63%, 100%, and 82%, respectively. Further studies are needed to evaluate the diagnostic performance and, even more so, the clinical impact of EUS in comparison to MRCP. Nevertheless, EUS may be more accurate in certain situations, because it does not seem to be as dependent on stone size.76 On the basis of the discussed data, there is level 2A evidence supporting EUS as an accurate and a safe method for the detection of CBD stones. EUS is less invasive than ERCP84 and is able to detect small stones in non-dilated ducts.76,85 This technology does not expose the patient to radiation or GASTROINTESTINAL ENDOSCOPY
439
F Tse, J Barkun, A Barkun
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
Table 3. Studies of hCTC with n > 10 that provided data on the sensitivity, specificity, and accuracy of hCTC in the diagnosis of CBD stones* Investigator Kwon et al.95 Cabada et al.101 Soto et al.100 Van Beers et al.98 Stockberger et al.102 Maniatis et al.103 Weighted averagesy
Study type Prospective, Prospective, Prospective, Prospective, Prospective, Prospective,
non-random non-random non-random non-random non-random non-random
N
Prevalence (%)
440 101 51 19 18 33
11% 22% 51% 16% 39% 30%
Sensitivity (%)
Specificity (%)
Accuracy (%)
85% 96% 92% 66% 86% 90% 87%: 95% CI[84, 90]
97% 97% 92% 100% 100% 100% 97%: 95% CI[95, 98]
96% 97% 92% 96% 94% 97% 96%: 95% CI[94, 97]
hCTC, Helical CT cholangiography; CBD, common bile duct; CI, confidence interval. *ERCP, percutaneous transhepatic cholangiography, laparoscopic CBD exploration, or open CBD exploration used as reference standards. yWeighted averages were based on the total number of patients (n = 662); 95% CI were calculated by using the normal approximation of the binomial distribution.
to contrast material. Tissue sampling in the form of either biopsy specimens or biliary cytology also is possible. The drawbacks to EUS include the high operator dependency with a steep learning curve, equipment cost, unit availability, the inability to provide an immediate therapeutic solution to CBD stones when present, the need for conscious sedation, and a 2% failure rate.75 Visualization is limited to the nearest 8 to 10 cm depth from the probe, and imaging can be obscured by pneumobilia, surgical clips, calcifying pancreatitis, or a duodenal diverticulum.86 IVC Intravenous cholangiography uses contrast material injected into the blood stream that then is rapidly taken up by the liver and subsequently excreted into the biliary tree, providing a cholangiogram. Reported performance characteristics are highly variable, possibly because of differences in patient populations studied and/or to inconsistent reference standards. Published studies pertaining to IVC in patients undergoing LC reports sensitivities ranging from 68% to 100% and specificities of 66% to 99% for identifying CBD stones, when it is compared with ERCP, IOC, MRCP, and/or clinical follow-up (level 2A).87-91 Intravenous cholangiography is contraindicated in any patient with a known allergy to iodine or with renal impairment. Major reactions to the contrast material include hepatorenal toxicity, cardiopulmonary symptoms, hypotension, severe skin reactions, and anaphylaxis.92,93 The overall mortality rate is 1 in 3000 to 5000 examinations. Because of its potential risks and limited test characteristics, IVC cannot be widely recommended in the routine workup of CBD stones. hCTC Helical CT cholangiography involves the use of slip ring technology and the injection of intravenous 440
GASTROINTESTINAL ENDOSCOPY
contrast to acquire volumetric data for high-quality three-dimensional reconstructions of the biliary tree.53,94-97 It has the ability to opacify up to thirdorder intrahepatic ducts.98,99 Compared with direct imaging such as ERCP or IOC, hCTC achieved a sensitivity of 87%: 95% CI[84, 90], a specificity of 97%: 95% CI[95, 98], and an overall accuracy of 95%: 95% CI[94, 97] for the diagnosis of CBD stones.94-103 Table 3 summarizes the major studies that provided data on the sensitivity, the specificity, and the accuracy of hCTC in the diagnosis of CBD stones. Despite the relatively small number of patients in these series (n = 629), there is level 2A evidence to suggest that hCTC is more accurate than US and conventional CT in the diagnosis of CBD stones. However, hCTC may not be as good as direct methods imaging, such as ERCP or IOC, for CBD stones and has not been compared with EUS or MRCP, both of which do not expose the patient to ionizing radiation or contrast agents. The major advantages of hCTC over ERCP are its low level of invasiveness, operator independence, and low technical failure rate (1%), as well as provision of a three-dimensional understanding of the biliary tree. The major drawback of hCTC is a risk of adverse reaction to the iodinated contrast agents (1%), while its main limitation is in highgrade obstruction, because contrast is not eliminated well into the biliary tree.94,95 The artifacts produced by a patient’s movement or intolerance to apnea might also limit the diagnostic value of this test. IOUS Intra-operative US involves the use of linear-array transducers with frequencies of 7.5 to 10 MHz to image the ductal system. B-mode scanning and color Doppler capability are used to distinguish the bile ducts from vascular structures. Scanning is performed while the transducer is moved along the cystic VOLUME 60, NO. 3, 2004
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
F Tse, J Barkun, A Barkun
Table 4. Studies of IOUS during laparoscopic cholecystectomy with n > 50 that provided data on the sensitivity, specificity, PPV, and NPV of IOUS in the diagnosis of CBD stones Investigator Ohtani et al.31 Greig et al.105 Machi et al.28 Rothlin et al.25 Barteau et al.24 Tranter et al.104 Stiegmann et al.106 Siperstein et al.33 Thompson et al.27 Birth et al.35 Catheline et al.26 Weighted averages*
Study type Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective, Prospective,
non-random non-random non-random non-random non-random non-random non-random non-random non-random non-random non-random
N
Prevalence (%)
65 54 100 100 125 135 209 300 360 518 600
83% 13% 9% 4% 11% 36% 9% 9% 14% 5% 9%
Sensitivity (%)
Specificity (%)
80% 71% 89% 100% 71% 96% 90% 96% 90% 83% 80% 86%: 95% CI[85, 87]
98% 96% 100% 98% 100% 100% 100% 100% 100% 100% 99% 99%: 95% CI[98, 99]
PPV (%)
NPV (%)
80% 71% 100% 67% 100% 100% 100% 100% 100% 100% 89% 95%: 95% CI[94, 96]
98% 96% 99% 100% 96% 98% 99% 99% 98% 99% 99% 99%: 95% CI[98, 99]
IOUS, Intra-operative US; PPV, positive predictive value; NPV, negative predictive value; CI, confidence interval. *Weighted averages were based on the total number of patients (n = 2566); 95% CI were calculated by using the normal approximation of the binomial distribution.
duct and the hepatoduodenal ligament to the terminal end of the CBD. The intrahepatic ducts also can be visualized by placing the probe on the liver surface. Prospective controlled trials24-28,31-35,104-109 have shown IOUS to be equivalent to IOC in its ability to diagnose CBD stones accurately, with a sensitivity of 86%: 95% CI[85, 87] and a specificity of 99%: 95% CI[98, 99] (level 2A). The operating time also is shorter with IOUS (4.5-10.2 min) than with IOC (10.9-17.9 min).24-28,31,34,35,106,107,109 Table 4 summarizes the major studies of IOUS that have provided data on the sensitivity, the specificity, PPV, and NPV of IOUS in the diagnosis of CBD stones. The advantages of IOUS over IOC are a lack of adverse effects, unlimited repetition, lower costs, shorter examination times, and detection of coexisting intra-abdominal pathology. The disadvantages are technical difficulty, equipment availability, suboptimal visualization of the distal CBD, and operator dependency. Also, IOUS may be overly sensitive in detecting small stones and sludge, which are of questionable clinical significance.106,110,111 CONSIDERATIONS IN DETERMINING AN OPTIMAL APPROACH TO PATIENTS WITH SUSPECTED CBD STONES WHO ARE UNDERGOING LC Endoscopic vs. laparoscopic approach In the era of OC, IOC, followed, if needed, by open CBD exploration (OCBDE), was the strategy of choice for the management of CBD stones. Randomized trials failed to demonstrate a role for preoperative endoscopic management of patients with CBD stones who were scheduled for OC (level 1A).8-10 This was mainly because the morbidities of ERCP VOLUME 60, NO. 3, 2004
and OC were found to be cumulative. However, the recent widespread use of LC has prompted a reevaluation of the role of peri-operative ERCP. With the evolution of laparoscopic CBD exploration (LCBDE), successful clearance of the CBD can be achieved in 77% to 100% of cases by using LCBDE, with a complication rate of 12% and a mortality rate of 0% to 2%.11-13 Randomized controlled trials of LCBDE vs. pre-operative11,13 or post-operative ERCP12 have shown similar rates of duct clearance (75%-85%), with an advantage in duration of hospital stay for the LCBDE group (level 1A). However, the disparity in expertise and the highly variable availability of LCBDE remain a significant consideration, especially in light of comparable efficacy data from competent endoscopic management that is much more readily available. Predictors of CBD stones Although many of the indirect imaging tests discussed above (MRCP, EUS, and hCTC) appear promising, they are not always easily accessible, and there are few published studies with respect to their cost-effectiveness. The safest and least invasive initial biliary imaging test thus remains the transabdominal US, which is readily available.112 However, US exhibits only modest test performance at detecting CBD stones, with sensitivities in the range of 25% to 58% and specificities of 68% to 91% (level 2A).113-118 Proper selection of patients for further biliary imaging to exclude CBD stones is crucial to minimize patient morbidity and institutional cost. Clinical correlation with liver enzymes, as well as US findings, helps in establishing the pretest probability of CBD stones. A number of clinical algorithms80,119-130 have been proposed for risk GASTROINTESTINAL ENDOSCOPY
441
F Tse, J Barkun, A Barkun
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
stratification in patients with suspected CBD stones. Barkun et al.119 made use of patient age (>55), total bilirubin (>30 lmoles/L, or approximately 1.8 mg/ dL), and US findings (a dilated CBD, a CBD stone) to predict the probability of CBD stones in patients referred for ERCP. Depending on the presence or the absence of these parameters, the algorithm predicted probabilities of finding a bile duct stone at ERCP range from 18% (no predictor present, amidst a patient population that only included patients with some liver or pancreatic test abnormality), to 94% (all four predictors present).119 In the metaanalysis published by Abboud et al.,125 indicators with positive likelihood ratios of 10 or above were cholangitis, pre-operative jaundice, and US evidence of CBD stones. Positive likelihood ratios for dilated CBD on US, hyperbilirubinemia, and jaundice ranged from 4 to 7.125 Elevated levels of serum alkaline phosphatase, pancreatitis, cholecystitis, and hyperamylasemia exhibited positive likelihood ratios of less than 3.125 In a prospective study by Liu et al.,122 variables, including clinical evaluation (cholecystitis or pancreatitis), blood chemistries (alanine aminotransferase, aspartate aminotransferase, alkaline phosphatase, total bilirubin), and US findings (cholelithiasis, CBD size) were used to risk stratify patients undergoing LC into one of 4 groups (Group 1, extremely high; Group 2, high; Group 3, moderate; Group 4, low). Patients with cholelithiasis, a CBD of 5 mm or more, and liver enzyme elevation without clinical evidence of cholecystitis or biliary pancreatitis were assigned to Group 1 and underwent pre-operative ERCP. Patients with cholelithiasis, CBD diameter of 5 mm or more, and liver enzyme abnormalities in a context of clinical resolution, the presence of cholecystitis, or biliary pancreatitis were assigned to Group 2 and underwent MRCP. Patients with cholelithiasis, liver enzyme elevation, and a CBD less than 5 mm were assigned to Group 3 and underwent LC with IOC. Patients with cholelithiasis, a CBD less than 5 mm, and normal liver enzymes were assigned to Group 4 and underwent LC without IOC. This strategy resulted in the identification of CBD stones during pre-operative ERCP in 92.3% of the patients, and unsuspected CBD stones occurred in only 1.4% of patients. The ability of such algorithms80,119-124 to correctly classify patients into low likelihood (#10% probability), moderate likelihood (11%-55% probability), and high likelihood (>55% probability) of harboring CBDS were prospectively evaluated in a cohort of patients with suspected CBD stones.131 In this study, the algorithm devised by Barkun et al.119 was found to be the simplest, most inclusive, and accurate algorithm published to date in determining the likelihood of 442
GASTROINTESTINAL ENDOSCOPY
CBDS. On the basis of the mentioned data, there is level 1B evidence for the use of these clinical algorithms in stratifying patients with symptomatic cholelithiasis who would most likely benefit from further investigation to exclude CBD stones. Decision models, including cost-effectiveness studies Controversies surrounding the management of CBD stones in the LC era include the role of IOC,132 the need for and timing of ERCP,133-135 the role of newer biliary imaging technologies, and the optimal use of LCBDE.11-13,136 Given the large number of possible management strategies for patients with suspected CBD stones undergoing LC, it is extremely difficult to determine the optimal strategy with a single headto-head prospective trial.8,9,11-13,106 Many investigators have thus turned to decision modeling.29,137,138 Barkun et al.137 examined 5 clinical strategies in their decision analysis. The first 3 strategies used diagnostic IOC in patients at medium and high risk of having CBD stones and therapeutic modalities of OCBDE (Strategy A), LCBDE (Strategy B), or postoperative ERCP (Strategy C) if a stone was found. In the final two strategies (Strategies D and E), patients at high risk for CBD stones first underwent pre-operative ERCP, whereas patients at medium risk went to pre-operative ERCP (Strategy D) or to IOC (Strategy E). Patients at low risk for CBD stones proceeded directly to LC in all strategies. The global duration of hospital stay for 100 patients was used as the measure of effectiveness of each approach. Results were as follows: 650 days for IOC + OCBDE (Strategy A), 411 days for IOC + LCBDE (Strategy B), 397 days for ERCP in high- and medium-risk patients (Strategy D), 374 days for IOC + postoperative ERCP (Strategy C), and 355 days for ERCP in high and IOC in medium risk patients (Strategy E). When examining the performance of the strategies developed, two key clinical variables emerged that drive the conclusions of the model: (1) the pretest probability (i.e., population prevalence) of CBD stones, and (2) the level of expertise of the operator (endoscopist and/or laparoscopist). As the proportion of patients suspected of CBD stones increased, there was a predictable increase in total hospitalization in all strategies with no change in rank order. As the relative efficacy of laparoscopic or endoscopic stone removal increased, there was a predictable decrease in the global duration of hospital stay. Therefore, in this analysis, the strategy with the lowest global duration of hospital stay was one that used pre-operative ERCP in high-risk patients, IOC in intermediaterisk patients, and expectant management in lowVOLUME 60, NO. 3, 2004
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
F Tse, J Barkun, A Barkun
Figure 1. Results of a decision model: sensitivity analysis expressed as a function of hospital stay and stone clearance for endoscopic or laparoscopic approach to CBD stone.137 The point of intersection between a laparoscopic and an endoscopic approach to CBD stone suggests that endoscopic stone removal is favored if equal expertise is available with a stone clearance rate of 52% or greater.137
risk patients. The sensitivity analysis showed, given an equal stone clearance rate for endoscopic and laparoscopic approaches, that the endoscopic approach was favored when a clearance rate of 52% or greater could be achieved (Fig. 1). Published studies with respect to cost-effectiveness of the new biliary imaging modalities are limited. Sahai et al.29 evaluated 4 peri-LC strategies: ERCP, IOC, EUS, and expectant management in patients with suspected CBD stones in a decision analysis. Their results revealed that IOC, and the selective use of EUS was the least costly method, unless the pretest probability of CBD stones was less than 11%, in which case expectant management was favored, or greater than 55%, in which case, ERCP was favored. Neither IOC nor EUS appear likely to reduce overall costs unless their accuracy and success rates are greater than 90% and their procedural cost is less than 60% to 70% that of ERCP. If neither is available, ERCP is preferred when the risk of stones is greater than 22%. Urbach et al.30 evaluated 4 strategies for managing CBD stones around the time of LC: (1) routine pre-operative ERCP, (2) LC with IOC, followed by LCBDE, (3) LC with IOC, followed by postoperative ERCP, (4) LC without cholangiography. Laparoscopic CBD exploration was found to be the most cost-effective method. If expertise in LCBDE was unavailable, selective postoperative ERCP was preferred over routine pre-operative ERCP, unless the probability of CBD stones was extremely high (>80%).30 In summary, the most cost-effective approach to CBD stones must take into account the pretest probability of stones, as well as local availability and expertise (level 2B).139 Patients with the lowest VOLUME 60, NO. 3, 2004
Figure 2. A proposed algorithm for the management of patients with suspected choledocholithiasis before laparoscopic cholecystectomy.
risk of having CBD stones should proceed directly to LC with no cholangiography (level 2B). Pre-operative ERCP should be reserved for patients who are at high risk of having CBD stones (level 2B).4 For patients at intermediate risk of having CBD stones, the optimal approach seems to be IOC followed, if positive, by LCBDE or postoperative ERCP, depending on local expertise (level 2B). Alternatively, a strategy that involves pre-operative ERCP, EUS, or MRCP instead of IOC may be considered for patients at intermediate risk, depending on local availability, expertise, and cost issues (level 2B). A proposed algorithm for the management of patients with suspected CBD stones undergoing LC is shown in Figure 2 and presents many similarities to that recently proposed by the American Society for Gastrointestinal Endoscopy.139 The supporting evidence for all final recommendations is graded in Table 5. CONCLUSIONS AND FUTURE DIRECTIONS There has been a marked increase in the choice and the use of biliary imaging modalities in recent years. Yet, their respective roles are still somewhat unclear, as are their impacts on health economics. Real-life results may be different than what could be anticipated, based on test performance GASTROINTESTINAL ENDOSCOPY
443
F Tse, J Barkun, A Barkun
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
Table 5. Optimizing the approach to patients with suspected CBD stones undergoing laparoscopic cholecystectomy5,6 Clinical situation Routine use of IOC in patients undergoing OC or LC is not recommended Pre-operative ERCP is not recommended in the management of patients with known CBD stones before OC MRCP is accurate and safe in the detection of CBD stones EUS is accurate and safe in the detection of CBD stones IVC cannot be widely recommended in the routine work-up of patients with suspected CBD stones because of its potential risk and limited test characteristics hCTC cannot be widely recommended in the routine work-up of patients with suspected CBD stones because of its potential risk and limited test characteristics IOUS is accurate and safe in the detection of CBD stones Abdominal US is the most cost-effective initial imaging test in the work-up of patients with suspected CBD stones Predictive models are useful in stratifying the risk of patients bearing CBD stones Pre-operative ERCP should be reserved for patients undergoing LC with high risk of having CBD stones Patients with low probability of CBD stones should proceed to LC with no cholangiography The choice of IOC vs. pre-operative ERCP for patients with intermediate probability of CBD stones should be dictated by the availability of local expertise and cost EUS and MRCP may be used to evaluate patients with intermediate probability of CBD stones The choice of LCBDE vs. peri-operative ERCP for patients with CBD stones detected at the time of IOC should be dictated by the availability of local expertise and cost
Level of evidence
Grades of recommendation
1A 1A
A A
2A 2A 2A
B B B
2A
B
2A 2A
B B
1B 2B 2B 2B
A B B B
2B 1A
B A
CBD, Common bile duct; IOC, intra-operative cholangiogram; OC, open cholecystectomy; LC, laparoscopic cholecystectomy; IVC, intravenous cholangiography; hCTC, helical CT cholangiography; IOUS, intra-operative US; LCBDE, laparoscopic CBD exploration.
characteristics or decision modeling. Clinicians may be reluctant to direct clinical actions based solely on noninvasive biliary images, consequently ERCP often will be requested to confirm the findings, thereby adding to clinical costs and patient inconvenience. For example, coincident with the marked increase in the number of MRCPs performed for biliary obstruction at the Hopital Erasme in Brussels from 1995 to 1997, there was only a minor reduction in the total number of ERCPs (about 1 diagnostic or therapeutic ERCP less for every 4 additional MRCPs).140 Preliminary data from a prospective randomized trial141 from our group, comparing ERCP with MRCP, whose study population was, in the majority, composed of patients with suspected choledocholithiasis, suggested a high rate of subsequent ERCPs in the MRCP arm (51%), with no differences between the groups in terms of rate of subsequent complications or overall duration of hospital stay. In a recent prospective cohort study142 comparing the incremental cost-effectiveness of initial MRCP and initial EUS with initial ERCP in patients with suspected biliary disease, initial EUS and initial MRCP were found to be less costly than initial ERCP, but provider expertise, biliary disease prevalence, and procedural costs influenced incremental cost-effectiveness. More true outcome trials, therefore, are needed to better assess the impact on clinical decision making or patient outcomes of these new diagnostic methods. 444
GASTROINTESTINAL ENDOSCOPY
ACKNOWLEDGMENTS The authors would like to thank Drs. Neena Abraham, Janet Booth, Jeffrey Bornstein, Gad Friedman, Joe Romagnuolo, as well as Ms. Patrizia Papalia for their contribution to selected parts of this manuscript. REFERENCES 1. Hunter JG. Laparoscopic transcystic common bile duct exploration. Am J Surg 1992;163:53-6. 2. Cranley B, Logan H. Exploration of the common bile duct: the relevance of the clinical picture and the importance of peroperative cholangiography. Br J Surg 1980;67: 869-72. 3. Soltan HM, Kow L, Toouli J. A simple scoring system for predicting bile duct stones in patients with cholelithiasis. J Gastrointest Surg 2001;5:434-7. 4. National Institutes of Health Consensus Development Conference statement on gallstones and laparoscopic cholecystectomy. Am J Surg 1993;165:390-8. 5. Guyatt GH, Sackett DL, Sinclair JC, Hayward R, Cook DJ, Cook RJ. Users’ guides to the medical literature. IX. A method for grading health care recommendations. EvidenceBased Medicine Working Group. JAMA 1995;274:1800-4. 6. Ball C, Phillips R. Evidence-based on-call. London: Churchill Livingstone; 2002. 7. Frey CF, Burbige EJ, Meinke WB, Pullos TG, Wong HN, Hickman DM, et al. Endoscopic retrograde cholangiopancreatography. Am J Surg 1982;144:109-4. 8. Neoptolemos JP, Carr-Locke DL, Fossard DP. Prospective randomised study of preoperative endoscopic sphincterotomy versus surgery alone for common bile duct stones. Br Med J (Clin Res Ed) 1987;294:470-4. VOLUME 60, NO. 3, 2004
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
9. Stain SC, Cohen H, Tsuishoysha M, Donovan AJ. Choledocholithiasis Endoscopic sphincterotomy or common bile duct exploration. Ann Surg 1991;213:627-33. 10. Stiegmann GV, Goff JS, Mansour A, Pearlman N, Reveille RM, Norton L. Precholecystectomy endoscopic cholangiography and stone removal is not superior to cholecystectomy, cholangiography, and common duct exploration. Am J Surg 1992;163:227-30. 11. Cuschieri A, Lezoche E, Morino M, Croce E, Lacy A, Toouli J, et al. E.A.E.S. multicenter prospective randomized trial comparing two-stage vs single-stage management of patients with gallstone disease and ductal calculi. Surg Endosc 1999;13:952-7. 12. Rhodes M, Sussman L, Cohen L, Lewis MP. Randomised trial of laparoscopic exploration of common bile duct versus postoperative endoscopic retrograde cholangiography for common bile duct stones. Lancet 1998;351:159-61. 13. Sgourakis G, Karaliotas K. Laparoscopic common bile duct exploration and cholecystectomy versus endoscopic stone extraction and laparoscopic cholecystectomy for choledocholithiasis. A prospective randomized study. Minerva Chir 2002;57:467-74. 14. Leung JW, Neuhaus H, Chopita N. Mechanical lithotripsy in the common bile duct. Endoscopy 2001;33:800-4. 15. Van Dam J, Sivak MV Jr. Mechanical lithotripsy of large common bile duct stones. Cleve Clin J Med 1993;60:38-42. 16. Loperfido S, Angelini G, Benedetti G, Chilovi F, Costan F, De Berardinis F, et al. Major early complications from diagnostic and therapeutic ERCP: a prospective multicenter study. Gastrointest Endosc 1998;48:1-10. 17. Freeman ML, Nelson DB, Sherman S, Haber GB, Herman ME, Dorsher PJ, et al. Complications of endoscopic biliary sphincterotomy. N Engl J Med 1996;335:909-18. 18. Masci E, Toti G, Mariani A, Curioni S, Lomazzi A, Dinelli M, et al. Complications of diagnostic and therapeutic ERCP: a prospective multicenter study. Am J Gastroenterol 2001; 96:417-23. 19. Cotton PB, Lehman G, Vennes J, Geenen JE, Russell RC, Meyers WC, et al. Endoscopic sphincterotomy complications and their management: an attempt at consensus. Gastrointest Endosc 1991;37:383-93. 20. Sherman S, Ruffolo TA, Hawes RH, Lehman GA. Complications of endoscopic sphincterotomy. A prospective series with emphasis on the increased risk associated with sphincter of Oddi dysfunction and nondilated bile ducts. Gastroenterology 1991;101:1068-75. 21. Neuhaus H, Feussner H, Ungeheuer A, Hoffmann W, Siewert JR, Classen M. Prospective evaluation of the use of endoscopic retrograde cholangiography prior to laparoscopic cholecystectomy. Endoscopy 1992;24:745-9. 22. Cotton PB, Chung SC, Davis WZ, Gibson RM, Ransohoff DF, Strasberg SM. Issues in cholecystectomy and management of duct stones. Am J Gastroenterol 1994;89:S169-76. 23. NIH Consensus Conference. Gallstones and laparoscopic cholecystectomy. JAMA 1993;269:1018-24. 24. Barteau JA, Castro D, Arregui ME, Tetik C. A comparison of intraoperative ultrasound versus cholangiography in the evaluation of the common bile duct during laparoscopic cholecystectomy. Surg Endosc 1995;9:490-6. 25. Rothlin MA, Schob O, Schlumpf R, Largiader F. Laparoscopic ultrasonography during cholecystectomy. Br J Surg 1996;83:1512-6. 26. Catheline J, Rizk N, Champault G. A comparison of laparoscopic ultrasound versus cholangiography in the VOLUME 60, NO. 3, 2004
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
F Tse, J Barkun, A Barkun
evaluation of the biliary tree during laparoscopic cholecystectomy. Eur J Ultrasound 1999;10:1-9. Thompson DM, Arregui ME, Tetik C, Madden MT, Wegener M. A comparison of laparoscopic ultrasound with digital fluorocholangiography for detecting choledocholithiasis during laparoscopic cholecystectomy. Surg Endosc 1998;12: 929-32. Machi J, Tateishi T, Oishi AJ, Furumoto NL, Oishi RH, Uchida S, et al. Laparoscopic ultrasonography versus operative cholangiography during laparoscopic cholecystectomy: review of the literature and a comparison with open intraoperative ultrasonography. J Am Coll Surg 1999;188: 360-7. Sahai AV, Mauldin PD, Marsi V, Hawes RH, Hoffman BJ. Bile duct stones and laparoscopic cholecystectomy: a decision analysis to assess the roles of intraoperative cholangiography, EUS, and ERCP. Gastrointest Endosc 1999;49:334-43. Urbach DR, Khajanchee YS, Jobe BA, Standage BA, Hansen PD, Swanstrom LL. Cost-effective management of common bile duct stones: a decision analysis of the use of endoscopic retrograde cholangiopancreatography (ERCP), intraoperative cholangiography, and laparoscopic bile duct exploration. Surg Endosc 2001;15:4-13. Ohtani T, Kawai C, Shirai Y, Kawakami K, Yoshida K, Hatakeyama K. Intraoperative ultrasonography versus cholangiography during laparoscopic cholecystectomy: a prospective comparative study. J Am Coll Surg 1997;185: 274-82. Flowers JL, Zucker KA, Graham SM, Scovill WA, Imbembo AL, Bailey RW. Laparoscopic cholangiography. Results and indications. Ann Surg 1992;215:209-16. Siperstein A, Pearl J, Macho J, Hansen P, Gitomirsky A, Rogers S. Comparison of laparoscopic ultrasonography and fluorocholangiography in 300 patients undergoing laparoscopic cholecystectomy. Surg Endosc 1999;13:113-7. Pietrabissa A, Di Candio G, Giulianotti PC, Shimi SM, Cuschieri A, Mosca F. Comparative evaluation of contact ultrasonography and transcystic cholangiography during laparoscopic cholecystectomy: a prospective study. Arch Surg 1995;130:1110-4. Birth M, Ehlers KU, Delinikolas K, Weiser HF. Prospective randomized comparison of laparoscopic ultrasonography using a flexible-tip ultrasound probe and intraoperative dynamic cholangiography during laparoscopic cholecystectomy. Surg Endosc 1998;12:30-6. Soper NJ, Dunnegan DL. Routine versus selective intraoperative cholangiography during laparoscopic cholecystectomy. World J Surg 1992;16:1133-40. Flum DR, Flowers C, Veenstra DL. A cost-effectiveness analysis of intraoperative cholangiography in the prevention of bile duct injury during laparoscopic cholecystectomy. J Am Coll Surg 2003;196:385-93. Ludwig K, Bernhardt J, Steffen H, Lorenz D. Contribution of intraoperative cholangiography to incidence and outcome of common bile duct injuries during laparoscopic cholecystectomy. Surg Endosc 2002;16:1098-104. Bagnato VJ, McGee GE, Hatten LE, Varner JE, Culpepper JP III. Justification for routine cholangiography during laparoscopic cholecystectomy. Surg Laparosc Endosc 1991; 1:89-93. Sackier JM, Berci G, Phillips E, Carroll B, Shapiro S, PazPartlow M. The role of cholangiography in laparoscopic cholecystectomy. Arch Surg 1991;126:1021-5. Millat B, Deleuze A, de Saxce B, De Seguin C, Fingerhut A. Routine intraoperative cholangiography is feasible and GASTROINTESTINAL ENDOSCOPY
445
F Tse, J Barkun, A Barkun
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52. 53. 54. 55.
56.
57.
58.
59.
446
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
efficient during laparoscopic cholecystectomy. Hepatogastroenterology 1997;44:22-7. Snow LL, Weinstein LS, Hannon JK, Lane DR. Evaluation of operative cholangiography in 2043 patients undergoing laparoscopic cholecystectomy: a case for the selective operative cholangiogram. Surg Endosc 2001;15:14-20. Csendes A, Burdiles P, Diaz JC, Maluenda F, Korn O, Vallejo E, et al. Prevalence of common bile duct stones according to the increasing number of risk factors present. A prospective study employing routinely intraoperative cholangiography in 477 cases. Hepatogastroenterology 1998;45:1415-21. Barkun JS, Fried GM, Barkun AN, Sigman HH, Hinchey EJ, Garzon J, et al. Cholecystectomy without operative cholangiography. Implications for common bile duct injury and retained common bile duct stones. Ann Surg 1993;218:371-7. Hauer-Jensen M, Karesen R, Nygaard K, Solheim K, Amlie EJ, Havig O, et al. Prospective randomized study of routine intraoperative cholangiography during open cholecystectomy: long-term follow-up and multivariate analysis of predictors of choledocholithiasis. Surgery 1993;113:318-23. Flum DR, Dellinger EP, Cheadle A, Chan L, Koepsell T. Intraoperative cholangiography and risk of common bile duct injury during cholecystectomy. JAMA 2003;289: 1639-44. Flum DR, Koepsell T, Heagerty P, Sinanan M, Dellinger EP. Common bile duct injury during laparoscopic cholecystectomy and the use of intraoperative cholangiography: adverse outcome or preventable error? Arch Surg 2001; 136:1287-92. Teplick SK, Haskin PH, Matsumoto T, Wolferth CC Jr, Pavlides CA, Gain T. Interventional radiology of the biliary system and pancreas. Surg Clin North Am 1984;64:87-119. Cotton PB, Speer AG. Risks and benefits of percutaneous transhepatic biliary drainage. Gastroenterology 1987;93: 667-8. Speer AG, Cotton PB, Russell RC, Mason RR, Hatfield AR, Leung JW, et al. Randomised trial of endoscopic versus percutaneous stent insertion in malignant obstructive jaundice. Lancet 1987;II:57-62. Dowsett JF, Vaira D, Hatfield AR, Cairns SR, Polydorou A, Frost R, et al. Endoscopic biliary therapy using the combined percutaneous and endoscopic technique. Gastroenterology 1989;96:1180-6. Coakley FV, Qayyum A. Magnetic resonance cholangiopancreatography. Gastrointest Endosc 2002;55:S2-12. Gillams AR, Lees WR. Recent developments in biliary tract imaging. Gastrointest Endosc Clin N Am 1996;6:1-15. Outwater EK, Gordon SJ. Imaging the pancreatic and biliary ducts with MR. Radiology 1994;192:19-21. Dubno B, Debatin JF, Luboldt W, Schmidt M, Hany TF, Bauerfeind P, Virtual MR cholangiography. AJR Am J Roentgenol 1998;171:1547-50. Fulcher AS, Turner MA, Capps GW, Zfass AM, Baker KM. Half-Fourier RARE MR cholangiopancreatography: experience in 300 subjects. Radiology 1998;207:21-32. Guibaud L, Bret PM, Reinhold C, Atri M, Barkun AN. Bile duct obstruction and choledocholithiasis: diagnosis with MR cholangiography. Radiology 1995;197:109-15. Reinbold C, Bret PM, Guibaud L, Barkun AN, Genin G, Atri M. MR cholangiopancreatography: potential clinical applications. Radiographics 1996;16:309-20. Romagnuolo J, Bardou M, Rahme E, Joseph L, Reinhold C, Barkun AN. Magnetic resonance cholangiopancreatograGASTROINTESTINAL ENDOSCOPY
60.
61.
62.
63.
64.
65.
66.
67.
68.
69.
70.
71.
72.
73. 74.
75.
phy: a meta-analysis of test performance in suspected biliary disease. Ann Intern Med 2003;139:547-57. Mendler MH, Bouillet P, Sautereau D, Chaumerliac P, Cessot F, Le Sidaner A, et al. Value of MR cholangiography in the diagnosis of obstructive diseases of the biliary tree: a study of 58 cases. Am J Gastroenterol 1998;93:2482-90. Boraschi P, Neri E, Braccini G, Gigoni R, Caramella D, Perri G, et al. Choledocolithiasis: diagnostic accuracy of MR cholangiopancreatography. Three-year experience. Magn Reson Imaging 1999;17:1245-53. Zidi SH, Prat F, Le Guen O, Rondeau Y, Rocher L, Fritsch J, et al. Use of magnetic resonance cholangiography in the diagnosis of choledocholithiasis: prospective comparison with a reference imaging method. Gut 1999;44: 118-22. Sugiyama M, Atomi Y, Hachiya J. Magnetic resonance cholangiography using half-Fourier acquisition for diagnosing choledocholithiasis. Am J Gastroenterol 1998;93: 1886-90. Little AF, Smith PJ, Lee WK, Hennessy OF, Desmond PV, Banting SW, et al. Imaging of the normal and abnormal pancreaticobiliary system with single-shot MR cholangiopancreatography: a pictorial review. Australas Radiol 1999; 43:427-34. Griffin N, Wastle ML, Dunn WK, Ryder SD, Beckingham IJ. Magnetic resonance cholangiopancreatography versus endoscopic retrograde cholangiopancreatography in the diagnosis of choledocholithiasis. Eur J Gastroenterol Hepatol 2003;15:809-13. Watanabe Y, Dohke M, Ishimori T, Amoh Y, Okumura A, Oda K, et al. Diagnostic pitfalls of MR cholangiopancreatography in the evaluation of the biliary tract and gallbladder. Radiographics 1999;19:415-29. Watanabe Y, Dohke M, Ishimori T, Amoh Y, Okumura A, Oda K, et al. Pseudo-obstruction of the extrahepatic bile duct due to artifact from arterial pulsatile compression: a diagnostic pitfall of MR cholangiopancreatography. Radiology 2000;214:856-60. Sugita R, Sugimura E, Itoh M, Ohisa T, Takahashi S, Fujita N. Pseudolesion of the bile duct caused by flow effect: a diagnostic pitfall of MR cholangiopancreatography. AJR Am J Roentgenol 2003;180:467-71. Becker CD, Grossholz M, Becker M, Mentha G, de Peyer R, Terrier F. Choledocholithiasis and bile duct stenosis: diagnostic accuracy of MR cholangiopancreatography. Radiology 1997;205:523-30. David V, Reinhold C, Hochman M, Chuttani R, McKee J, Waxman I, et al. Pitfalls in the interpretation of MR cholangiopancreatography. AJR Am J Roentgenol 1998; 170:1055-9. Hall-Craggs MA, Allen CM, Owens CM, Theis BA, Donald JJ, Paley M, et al. MR cholangiography: clinical evaluation in 40 cases. Radiology 1993;189:423-7. Amouyal P, Amouyal G, Levy P, Tuzet S, Palazzo L, Vilgrain V, et al. Diagnosis of choledocholithiasis by endoscopic ultrasonography. Gastroenterology 1994;106:1062-7. Sivak MV Jr. EUS for bile duct stones: how does it compare with ERCP? Gastrointest Endosc 2002;56:S175-7. Buscarini E, Tansini P, Vallisa D, Zambelli A, Buscarini L. EUS for suspected choledocholithiasis: do benefits outweigh costs? A prospective, controlled study. Gastrointest Endosc 2003;57:510-8. Palazzo L, Girollet PP, Salmeron M, Silvain C, Roseau G, Canard JM, et al. Value of endoscopic ultrasonography in the diagnosis of common bile duct stones: comparison with VOLUME 60, NO. 3, 2004
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
76.
77.
78.
79.
80.
81.
82.
83.
84.
85.
86.
87.
88.
89.
90.
91.
surgical exploration and ERCP. Gastrointest Endosc 1995;42:225-31. Sugiyama M, Atomi Y. Endoscopic ultrasonography for diagnosing choledocholithiasis: a prospective comparative study with ultrasonography and computed tomography. Gastrointest Endosc 1997;45:143-6. Kohut M, Nowakowska-Dulawa E, Marek T, Kaczor R, Nowak A. Accuracy of linear endoscopic ultrasonography in the evaluation of patients with suspected common bile duct stones. Endoscopy 2002;34:299-303. Shim CS, Joo JH, Park CW, Kim YS, Lee JS, Lee MS, et al. Effectiveness of endoscopic ultrasonography in the diagnosis of choledocholithiasis prior to laparoscopic cholecystectomy. Endoscopy 1995;27:428-32. Prat F, Amouyal G, Amouyal P, Pelletier G, Fritsch J, Choury AD, et al. Prospective controlled study of endoscopic ultrasonography and endoscopic retrograde cholangiography in patients with suspected common-bileduct lithiasis. Lancet 1996;347:75-9. Canto MI, Chak A, Stellato T, Sivak MV Jr. Endoscopic ultrasonography versus cholangiography for the diagnosis of choledocholithiasis. Gastrointest Endosc 1998;47:439-48. Norton SA, Alderson D. Prospective comparison of endoscopic ultrasonography and endoscopic retrograde cholangiopancreatography in the detection of bile duct stones. Br J Surg 1997;84:1366-9. Napoleon B, Dumortier J, Keriven-Souquet O, Pujol B, Ponchon T, Souquet JC. Do normal findings at biliary endoscopic ultrasonography obviate the need for endoscopic retrograde cholangiography in patients with suspicion of common bile duct stone? A prospective follow-up study of 238 patients. Endoscopy 2003;35:411-5. de Ledinghen V, Lecesne R, Raymond JM, Gense V, Amouretti M, Drouillard J, et al. Diagnosis of choledocholithiasis: EUS or magnetic resonance cholangiography? A prospective controlled study. Gastrointest Endosc 1999; 49:26-31. Ro¨sch T, Dittler HJ, Fockens P, Yasuda K, Lightdale C. Major complications of endoscopic ultrasonography: results of a survey of 42,105 cases [abstract]. Gastrointest Endosc 1993;39:341. Liu CL, Lo CM, Chan JK, Poon RT, Fan ST. EUS for detection of occult cholelithiasis in patients with idiopathic pancreatitis. Gastrointest Endosc 2000;51:28-32. Deprez P. Approach of suspected common bile duct stones: endoscopic ultrasonography. Acta Gastroenterol Belg 2000; 63:295-8. Khan AL, Miller SS. Intravenous cholangiography and operative cholangiography: implications for laparoscopic cholecystectomy. J R Coll Surg Edinb 1995;40:233-6. Lindsey I, Nottle PD, Sacharias N. Preoperative screening for common bile duct stones with infusion cholangiography: review of 1000 patients. Ann Surg 1997;226:174-8. Dorenbusch MJ, Maglinte DD, Micon LT, Graffis RA, Turner WW Jr. Intravenous cholangiography and the management of choledocholithiasis prior to laparoscopic cholecystectomy. Surg Laparosc Endosc 1995;5:188-92. Joyce WP, Keane R, Burke GJ, Daly M, Drumm J, Egan TJ, et al. Identification of bile duct stones in patients undergoing laparoscopic cholecystectomy. Br J Surg 1991;78: 1174-6. Reuther G, Kiefer B, Tuchmann A. Cholangiography before biliary surgery: single-shot MR cholangiography versus intravenous cholangiography. Radiology 1996;198:561-6.
VOLUME 60, NO. 3, 2004
F Tse, J Barkun, A Barkun
92. Ott DJ, Gelfand DW. Complications of gastrointestinal radiologic procedures. II. Complications related to biliary tract studies. Gastrointest Radiol 1981;6:47-56. 93. Adam A, Bowley NB. The biliary tract. In: Grainger RG, Allison DJ, editors. Grainger and AllisonÕs diagnostic radiology. 3rd ed. New York: Churchill Livingston; 1992. p. 1077-110. 94. Heiken JP, Brink JA, Vannier MW. Spiral (helical) CT. Radiology 1993;189:647-56. 95. Kwon AH, Uetsuji S, Yamada O, Inoue T, Kamiyama Y, Boku T. Three-dimensional reconstruction of the biliary tract using spiral computed tomography. Br J Surg 1995;82:260-3. 96. Goldberg HI. Helical cholangiography: complementary or substitute study for endoscopic retrograde cholangiography? Radiology 1994;192:615-6. 97. Klein HM, Wein B, Truong S, Pfingsten FP, Gunther RW. Computed tomographic cholangiography using spiral scanning and 3D image processing. Br J Radiol 1993;66:762-7. 98. van Beers BE, Lacrosse M, Trigaux JP, de Canniere L, De Ronde T, Pringot J. Noninvasive imaging of the biliary tree before or after laparoscopic cholecystectomy: use of threedimensional spiral CT cholangiography. AJR Am J Roentgenol 1994;162:1331-5. 99. Fleischmann D, Ringl H, Schofl R, Potzi R, Kontrus M, Henk C, et al. Three-dimensional spiral CT cholangiography in patients with suspected obstructive biliary disease: comparison with endoscopic retrograde cholangiography. Radiology 1996;198:861-8. 100. Soto JA, Alvarez O, Munera F, Velez SM, Valencia J, Ramirez N. Diagnosing bile duct stones: comparison of unenhanced helical CT, oral contrast-enhanced CT cholangiography, and MR cholangiography. AJR Am J Roentgenol 2000;175:1127-34. 101. Cabada Giadas T, Sarria Octavio de Toledo L, MartinezBerganza Asensio MT, Cozcolluela Cabrejas R, Alberdi Ibanez I, Alvarez Lopez A, et al. Helical CT cholangiography in the evaluation of the biliary tract: application to the diagnosis of choledocholithiasis. Abdom Imaging 2002;27:61-70. 102. Stockberger SM, Wass JL, Sherman S, Lehman GA, Kopecky KK. Intravenous cholangiography with helical CT: comparison with endoscopic retrograde cholangiography. Radiology 1994;192:675-80. 103. Maniatis P, Triantopoulou C, Sofianou E, Siafas I, Psatha E, Dervenis C, et al. Virtual CT cholangiography in patients with choledocholithiasis. Abdom Imaging 2003;28:536-44. 104. Tranter SE, Thompson MH. A prospective single-blinded controlled study comparing laparoscopic ultrasound of the common bile duct with operative cholangiography. Surg Endosc 2003;17:216-9. 105. Greig JD, John TG, Mahadaven M, Garden OJ. Laparoscopic ultrasonography in the evaluation of the biliary tree during laparoscopic cholecystectomy. Br J Surg 1994;81: 1202-6. 106. Stiegmann GV, Soper NJ, Filipi CJ, McIntyre RC, Callery MP, Cordova JF. Laparoscopic ultrasonography as compared with static or dynamic cholangiography at laparoscopic cholecystectomy. A prospective multicenter trial. Surg Endosc 1995;9:1269-73. 107. Falcone RA Jr, Fegelman EJ, Nussbaum MS, Brown DL, Bebbe TM, Merhar GL, et al. A prospective comparison of laparoscopic ultrasound vs intraoperative cholangiogram during laparoscopic cholecystectomy. Surg Endosc 1999; 13:784-8. 108. Yamashita Y, Kurohiji T, Hayashi J, Kimitsuki H, Hiraki M, Kakegawa T. Intraoperative ultrasonography during GASTROINTESTINAL ENDOSCOPY
447
F Tse, J Barkun, A Barkun
109.
110.
111.
112.
113.
114.
115.
116.
117. 118.
119.
120.
121.
122.
123.
124.
125.
448
Laparoscopic cholecystectomy: elective evaluation of suspected choledocholithiasis
laparoscopic cholecystectomy. Surg Laparosc Endosc 1993; 3:167-71. Goletti O, Buccianti P, Decanini L, Lippolis PV, Spisni R, Chiarugi M, et al. Intraoperative sonography of biliary tree during laparoscopic cholecystectomy. Surg Laparosc Endosc 1994;4:9-12. Wu JS, Dunnegan DL, Soper NJ. The utility of intracorporeal ultrasonography for screening of the bile duct during laparoscopic cholecystectomy. J Gastrointest Surg 1998;2:50-60. Teefey SA, Soper NJ, Middleton WD, Balfe DM, Brink JA, Strasberg SM, et al. Imaging of the common bile duct during laparoscopic cholecystectomy: sonography versus videofluoroscopic cholangiography. AJR Am J Roentgenol 1995; 165:847-51. Barkun JS, Barkun AN. Jaundice. In: Wilmore DW, Cheung LY, Harken AH, Holcroft JW, Meakins JL, Soper NJ, editors. ACS surgery: principles and practice 2003. New York: WebMD Professional Publishing; 2003. Sutton D. Ultrasound. In: Sutton D, editor. A textbook of radiology and imaging. 4th ed. Edinburgh: Churchill Livingston; 1987. p. 1773-809. Taylor KJ, Rosenfield AT, Spiro HM. Diagnostic accuracy of gray scale ultrasongraphy for the jaundiced patient. A report of 275 cases. Arch Intern Med 1979;139:60-3. Lapis JL, Orlando RC, Mittelstaedt CA, Staab EV. Ultrasonography in the diagnosis of obstructive jaundice. Ann Intern Med 1978;89:61-3. Morris A, Fawcitt RA, Wood R, Forbes WS, Isherwood I, Marsh MN. Computed tomography, ultrasound, and cholestatic jaundice. Gut 1978;19:685-8. Vallon AG, Lees WR, Cotton PB. Grey-scale ultrasonography in cholestatic jaundice. Gut 1979;20:51-4. Baron RL, Stanley RJ, Lee JK, Koehler RE, Melson GL, Balfe DM, et al. A prospective comparison of the evaluation of biliary obstruction using computed tomography and ultrasonography. Radiology 1982;145:91-8. Barkun AN, Barkun JS, Fried GM, Ghitulescu G, Steinmetz O, Pham C, et al. Useful predictors of bile duct stones in patients undergoing laparoscopic cholecystectomy. McGill Gallstone Treatment Group. Ann Surg 1994;220:32-9. Onken JE, Brazer SR, Eisen GM, Williams DM, Bouras EP, DeLong ER, et al. Predicting the presence of choledocholithiasis in patients with symptomatic cholelithiasis. Am J Gastroenterol 1996;91:762-7. Kim KH, Kim W, Lee HI, Sung CK. Prediction of common bile duct stones: its validation in laparoscopic cholecystectomy. Hepatogastroenterology 1997;44:1574-9. Liu TH, Consorti ET, Kawashima A, Tamm EP, Kwong KL, Gill BS, et al. Patient evaluation and management with selective use of magnetic resonance cholangiography and endoscopic retrograde cholangiopancreatography before laparoscopic cholecystectomy. Ann Surg 2001;234:33-40. Lacaine F, Corlette MB, Bismuth H. Preoperative evaluation of the risk of common bile duct stones. Arch Surg 1980;115:1114-6. Tham TC, Lichtenstein DR, Vandervoort J, Wong RC, Brooks D, Van Dam J, et al. Role of endoscopic retrograde cholangiopancreatography for suspected choledocholithiasis in patients undergoing laparoscopic cholecystectomy. Gastrointest Endosc 1998;47:50-6. Abboud PA, Malet PF, Berlin JA, Staroscik R, Cabana MD, Clarke JR, et al. Predictors of common bile duct stones prior to cholecystectomy: a meta-analysis. Gastrointest Endosc 1996;44:450-5.
GASTROINTESTINAL ENDOSCOPY
126. Prat F, Meduri B, Ducot B, Chiche R, Salimbeni-Bartolini R, Pelletier G. Prediction of common bile duct stones by noninvasive tests. Ann Surg 1999;229:362-8. 127. Trondsen E, Edwin B, Reiertsen O, Faerden AE, Fagertun H, Rosseland AR. Prediction of common bile duct stones prior to cholecystectomy: a prospective validation of a discriminant analysis function. Arch Surg 1998;133:162-6. 128. Roston AD, Jacobson IM. Evaluation of the pattern of liver tests and yield of cholangiography in symptomatic choledocholithiasis: a prospective study. Gastrointest Endosc 1997;45:394-9. 129. Kama NA, Atli M, Doganay M, Kologlu M, Reis E, Dolapci M. Practical recommendations for the prediction and management of common bile duct stones in patients with gallstones. Surg Endosc 2001;15:942-5. 130. Santucci L, Natalini G, Sarpi L, Fiorucci S, Solinas A, Morelli A. Selective endoscopic retrograde cholangiography and preoperative bile duct stone removal in patients scheduled for laparoscopic cholecystectomy: a prospective study. Am J Gastroenterol 1996;91:1326-30. 131. Jakribettuu VS, Gilliam JH, Pineau BC. Comparisons of five algorithms used to predict common bile duct stones [abstract]. Am J Gastroenterol 2001;96:588. 132. Lillemoe KD, Yeo CJ, Talamini MA, Wang BH, Pitt HA, Gadacz TR. Selective cholangiography. Current role in laparoscopic cholecystectomy. Ann Surg 1992;215:669-74. 133. Heinerman PM, Boeckl O, Pimpl W. Selective ERCP and preoperative stone removal in bile duct surgery. Ann Surg 1989;209:267-72. 134. Ponchon T, Bory R, Chavaillon A, Fouillet P. Biliary lithiasis: combined endoscopic and surgical treatment. Endoscopy 1989;21:15-8. 135. Van Stiegmann G, Pearlman NW, Goff JS, Sun JH, Norton LW. Endoscopic cholangiography and stone removal prior to cholecystectomy. A more cost-effective approach than operative duct exploration? Arch Surg 1989;124:787-9. 136. Kelley WE Jr, Sheridan VC. Laparoscopic choledochoscopy with a small-caliber endoscope. A safe and effective technique for laparoscopic common bile duct exploration. Surg Endosc 1995;9:293-6. 137. Barkun AN, Abraham NS, Barkun JS, Booth J, Fried GM, McCall C, et al. What is the optimal management of patients with suspected choledocholithiasis in the era of laparoscopic cholecystectomy [abstract]? Gastroenterology 1999;116:A4. 138. Erickson RA, Carlson B. The role of endoscopic retrograde cholangiopancreatography in patients with laparoscopic cholecystectomies. Gastroenterology 1995;109:252-63. 139. Eisen GM, Dominitz JA, Faigel DO, Goldstein JL, Kalloo AN, Petersen BT, et al. An annotated algorithm for the evaluation of choledocholithiasis. Gastrointest Endosc 2001; 53:864-6. 140. Deviere J, Matos C, Cremer M. The impact of magnetic resonance cholangiopancreatography on ERCP. Gastrointest Endosc 1999;50:136-40. 141. Romagnuolo J, Barkun AN, Joseph L, Reinhold C, Barkun JS. A randomized clinical trial comparing ERCP and MRCP in an effectiveness setting [abstract]. Gastrointest Endosc 2000;51:AB199. 142. Carlos RC, Scheiman JM, Hussain HK, Song JH, Francis IR, Fendrick AM. Making cost-effectiveness analyses clinically relevant: the effect of provider expertise and biliary disease prevalence on the economic comparison of alternative diagnostic strategies. Acad Radiol 2003;10:620-30.
VOLUME 60, NO. 3, 2004