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Intraoperative ultrasonography versus cholangiography during laparoscopic cholecystectomy: a prospective comparative study
Intraoperative Ultrasonography Versus Cholangiography During Laparoscopic Cholecystectomy: A Prospective Comparative Study Tetsuya Ohtani, MD,* Chihiro Kawai, MD, + Yoshio Shirai, ILazutake Kawakami, MD, t Keisuke Yoshida, MD, -~ and Katsuyoshi Hatakeyama, MD* Background: The purpose of this study was to compare
were 80, 98, 80, 98, and 97% by IOUS, and 80, 97, 67, 98, and 95% by IOC, respectively.
the functional utility of intraoperative ultrasonography (IOUS) and cholangiography (IOC) during a laparoscopic cholecystectomy for the treatment of gallstone disease.
Conclusions: Intraoperative ultrasonography is superior to cholangiography with respect to its safety, shorter examination period, and ease of administration in all patients. In addition, IOUS is also better for identifying subtle anatomic detail. Intraoperative ultrasonography compares favorably with IOC in terms of utility in exploring bile ducts for stones. Intraoperative ultrasonography is an effective procedure for biliary exploration during a laparoscopic cholecystectomy. (J Am Coil Surg 1997;185:274-282. © 1997 by the American College of Surgeons)
Study Design:A prospective study comparing IOUS and IOC was carried out in 65 patients. Intraoperative ultrasonography was conducted first using a 7.5-MHz linear array probe. After IOUS, IOC was then conducted in all patients. The respective usefulness of IOUS and IOC in the identification of gallstones, detection of hepatobiliary structures, and demonstration of congenital anomalies was then compared. Results: Intraoperative ultrasonography was successful in all 65 patients, and IOC was successful only in 54. The time required for IOUS was significantly shorter (p < 0.0001) than for IOC. Intraoperative ultrasonography imaged the hepatic ducts and their confluence, the common hepatic duct, the common bile duct, and the ampulla of Vater in 97, 100, 97, and 51% of cases, respectively. Intraoperative cholangiography, on the other hand, depicted these structures in 85, 89, 100, and 94% of cases, respectively. Intraoperative ultrasonography demonstrated the cystic duct and its confluence in 94% of cases. Biliary anomalies were identified by IOUS in 12 patients and by IOC in 13. Intraoperative ultrasonography could detect the hilar vascular structures in most patients and visualized anomalies of the hepatic arteries in 5 patients. In this series, 5 patients had choledocholithiasis. The sensitivities, speciflcities, positive and negative predictive values, and accuracies in identifying these bile duct stones ReceivedJanuary 13, 1997;AcceptedMarch 24, 1997. From the *Departmentof Surgery,NiigataUniversitySchoolof Medicine, and the tDepartment of Surgery,The Nippon Dental University, Niigata,Japan. This work was supported in part by a Grant-in-Aid for Scientific Research (C) fromthe Ministryof Education,Science,and Cultureof Japan, accountno. 07671373. Correspondence address: TetsuyaOhtani, MD, Departmentof Surgee/, Niigata UniversitySchool of Medicine, 1-757Asahimachi-dori, Niigata, 951,Japan. © 1997 by the AmericanCollegeof Surgeons Published by ElsevierScienceInc.
MD,*
Intraoperative c h o l a n g i o g r a p h y (IOC) for gallstone disease d u r i n g an o p e n cholecystectomy has b e e n very useful in detecting u n s u s p e c t e d bile d u c t stones a n d anomalies of the biliary system. This p r o c e d u r e , however, has disadvantages including a high percentage of false-positive cholangiograms a n d a lengthy operative time a n d high cost (1). In the era of the laparoscopic cholecystectomy, r o u t i n e or selected IOC has thus b e c o m e controversial (2-4). T h e prevalence of bile d u c t stones, however, must n o t be disregarded, as they are f o u n d in 7-20% of patients with c o n c o m i t a n t gallbladder stones (5). Intraoperative screening for choledocholithiasis is therefore crucial, because this enables the surgeons to use several t r e a t m e n t options laparoscopically at the time of surgery, a n d as a result, avoid unnecessary postoperative intervention. T h e clinical use o f real-time B m o d e ultrasonography for gallstone disease was first described by Lane a n d colleagues (6), and Sigel and colleagues (7). They have reported that intraoperative ultrasonography (IOUS) was a reliable m e t h o d for detecting bile duct stones during an open cholecystectomy and demonstrated several advantages of IOUS compared with IOC (6, 7). The use of IOUS during a laparoscopic cholecystectomy was first reported by Jakimowicz (8), and recently some authors have de-
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FIG l. Transverse scans of linear array ultrasonography on the hepatoduodenal ligament through the epigastric port. (A) The ultrasonography demonstrates the cystic duct and common hepatic duct. (B) The cystic duct is clearly seen entering the common bile duct. (C) The intrapancreatic part of the common bile duct is visualized. (D) Ampulla of Vater and d u o d e n u m are demonstrated. CD, cystic duct; CHD, common hepatic duct; CBD, common bile duct; Panc, pancreas; DU, duodenum; Am, ampulla of Vater; PV, portal vein; IVC, inferior vena cava.
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scribed more specifically the operative technique and clinical indications (9-11). In our study, we have prospectively evaluated the effectiveness of IOUS and IOC for the detection of choledocholithiasis and hepatobiliary anatomic structures and anomaries during a laparoscopic cholecystectomy. Me~o~
Patient population. From J u n e 1993 to September 1994, 68 consecutive patients with suspected gallstone disease were referred to our institution. A laparoscopic cholecystectomy was a t t e m p t e d in all patients. Preoperative assessment consisted of obtaining a complete history; physical examination; transabdominal ultrasonography; liver function tests including measurements of serum bilirubin, asparate aminotransferase, alanine aminotransferase, and alkaline phosphatase; and a serum amylase level. Every patient's clinical course was carefully followed and recorded. Technique of laparoscopic cholecystectomy and intraoperative studies. Laparoscopic cholecystectomy was p e r f o r m e d using a standard four-puncture technique. After establishing p n e u m o p e r i t o n e u m , a 10 m m umbilical trocar was inserted into the peritoneal cavity. While carefully inspecting the abdominal cavity with the laparoscope, a 10 m m trocar in the epigastrium, a 5 m m trocar in the right midclavicular line, a n d a 5 m m trocar in the anterior axillar line were inserted. Before u l t r a s o n o g r a p h i c e x a m i n a t i o n , sterile saline was instilled into the peritoneal cavity over the hepat o d u o d e n a l ligament in order to provide an appropriate acoustic window. If structures were adh e r e n t to the gallbladder, they were dissected first. The ultrasonographic probe was then i n t r o d u c e d t h r o u g h the epigastric p o r t u n d e r direct visualization, with the laparoscope functioning t h r o u g h t h e umbilical port. T h e gallbladder wall and its contents were visualized t h r o u g h the liver parenchyma using the ultrasonographic probe. W h e n the probe was moved on the liver medially, the anterior and posterior branches of the portal pedicle and its j u n c t i o n were demonstrated. T h e probe was then positioned to the lateral surface of the liver to the right of the h e p a t o d u o d e n a l ligament. W h e n the probe was dragged down laterally to the right of the h e p a t o d u o d e n a l ligament and rotated clockwise, the transverse planes of the extrahepatic bile duct, p r o p e r hepatic artery, and portal vein were visualized in their entirety (Fig. 1). T h e ultrasonographic probe was subsequently introd u c e d u n d e r direct visualization into the umbilical port, with the laparoscope functioning in the epi-
FIG 2. Longitudinal scans of linear array ultrasonography through the umbilical port. The ultrasound scan clearly demonstrates the cysticduct entering the common bile duct. The right hepatic artery is seen between the common hepatic duct and the portal vein. CD, cystic duct; CHD, common hepatic duct; PV, portal vein; RHA, right hepatic artery; IVC, inferior vena cava.
gastric port. The longitudinal planes of the bile duct, portal vein, and inferior vena cava were then d e m o n s t r a t e d through the liver parenchyma and by direct contact with the h e p a t o d u o d e n a l ligam e n t (Fig. 2). T h e transverse plane of the right hepatic artery, lying between the extrahepatic bile duct a n d portal vein, was d e m o n s t r a t e d in the hepatic hilum using this technique (Fig. 2). Intraoperative ultrasonographic imaging was perf o r m e d using a 7.5 MHz lineal array transducer of the Aloka laparoscopic ultrasonographic probe (UST-5522-7.5, Aloka Co Ltd., Tokyo, Japan). An ultrasound scanner, the Aloka SSD 1200 (Aloka Co Ltd., Tokyo, Japan), was also used in this investigation. After completing the IOUS, the triangle of Callot was then dissected with cephalad traction on the gallbladder fundus and lateral traction on the infundibulum. The cystic duct was identified and freed entirely and then secured by a clip placed close to the gallbladder. Intraoperative cholangiography was carried o u t with the Olsen
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cholangiography fixation clamp (Karl Storz Endoscopy, Culver City, CA). The clamp was inserted through either epigastric port or the port located in the right anterior axillar line. We routinely infused 5-10 mL of contrast material (Urografin, Schering Corp., Osaka, Japan) in order to demonstrate duodenal flow of the contrast material. The duodenal papilla was visualized using fluoroscopy (Model TVM-128 = KN, Toshiba Corp., Kawasaki, Japan). Additional contrast material (5-10 mL) was then infused through the catheter, and x-ray films were obtained in order to detect choledocholithiasis. A cholecystectomy was performed only after dissection of the cystic duct and artery was complete, and after the intraoperative studies described above. The cholecystectomy was completed using electrocautery dissection, and the resected gallbladder was removed through the epigastric trocar.
Comparative studies between intraoperative ultrasonogTaphy and cholangiography. A prospective comparative study was undertaken to evaluate IOUS and IOC in identifying bile duct stones, hepatobiliary anatomic details, and congenital anomalies. The durations of these two examinations were compared in order to evaluate their feasibility. Intraoperative ultrasound was evaluated in terms of its accuracy in demonstrating anatomic details. The anatomic sites that were evaluated with IOUS included the following: the hepatic ducts and confluence, the c o m m o n hepatic duct, the c o m m o n bile duct, the cystic duct, the cystic d u c t confluence, the ampulla of Vater, the proper hepatic artery, the right hepatic artery, the cystic artery, and the portal vein (Figs. 1 and 2). Arteries were distinguished from other structures by the presence of pulsation. Detailed descriptive records were kept on patients who had bile duct stones or anomalies of the biliary system and hepatic arteries. A sharp echo with an acoustic shadow in the bile duct was defined as positive for a bile duct stone. The time required for IOUS was measured from the initial introduction of the probe to its removal from the trocar. Intraoperative cholangiography visualizing the biliary tree with contrast material was then carried out. The intrabiliary sites visualized by cholangiography included the following: the intrahepatic bile ducts, the hepatic ducts and confluence, the c o m m o n hepatic duct, the c o m m o n bile duct, and the ampulla of Vater. Specific points of interest during cholangiography were the presence or absence of filling defects and the identification of bile duct anomalies. A contrast-filling defect in the bile duct was defined as positive for a bile duct stone. The time required
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for IOC was measured from the initial clipping of the gallbladder site to the biliary ductal display on the film illuminator. Laparoscopic cholecystect0my was performed by three of the authors (TO, CK, and KK). The preoperative transabdominal ultrasonography, IOUS, and IOC were carried out by one surgeon (TO) experienced in ultrasonography. The two groups were compared statistically using the Student's unpaired t-test. Sensitivity, specificity, predictive values, and accuracy for both groups were then calculated. Results
Patient characteristics. A laparoscopic cholecystectomy was attempted in all 68 patients r e f e r r e d to our institution, but conversion to an open procedure was necessary in 2 patients after examination by IOUS. In one patient with severe acute cholecystitis, uncontrolled bleeding of a liver bed laceration occurred during the dissection of Callot triangle and resulted in conversion to an open cholecystectomy. In another patient, an incarcerated gallstone in the gallbladder neck provoked hydrops, and the gallbladder neck was closely adh e r e n t to the c o m m o n hepatic duct by IOUS. We therefore decided to proceed with an open cholecystectomy in order to prevent bile duct injury. The operation was completed laparoscopically in the remaining 66 patients (97%). In 1 of the 66 patients, a preoperative diagnosis of cholelithiasis was made, but only gallbladder polyps without stones .were identified by IOUS a n d later confirmed histologically. The 65 patients who had confirmed gallstones were entered into a prospective comparative study. Twenty-four patients were men and 41 patients were women. The average age of the group was 53.3 years (range, 20-85 years). Bile duct injury, bile leak, and vessel injury were observed neither during nor after laparoscopic cholecystectomy in these 65 patients. Previous abdominal operations had been performed in 26 of the 65 patients (39%); an upper abdominal incision was performed in 2 patients, and a lower abdominal incision in 25. The mean followup time after surgery was 23 months (range, 15-30 months). Intraoperative ultrasonographic study. Intraoperarive ultrasonography was tolerated in all 65 patients during the laparoscopic cholecystectomy. Before IOUS, lysis of the adhesions around the gallbladder was necessary in 17 patients, 2 patients seconda~y to previous abdominal surgery, and 15 secondary to inflammation related to cholecystitis.
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T a b l e 1. A n a t o m i c Sites Visualized by I n t r a o p e r a t i v e U l t r a s o n o g r a p h y in 65 P a t i e n t s
Extrahepatic bile ducts Hepatic ducts and confluence Common hepatic duct Common bile duct Cystic duct and confluence Ampulla of Vater Vessels Portal vein Proper hepatic artery Right hepatic artery Cystic artery
No. of patients
Percent
63 65 63 61 33
97 100 97 94 51
65 64 63 30
100 98 97 46
T h e m e a n e x a m i n a t i o n d u r a t i o n was 9.7 minutes (95% c o n f i d e n c e interval, 9.0-10.4 minutes). In one patient with acute cholecystitis, although the IOUS d e m o n s t r a t e d a gallbladder neck closely adh e r e n t to the c o m m o n hepatic duct, a laparoscopic cholecystectomy was c o m p l e t e d with careful dissection between the gallbladder n e c k a n d the c o m m o n hepatic duct. T h e ability o f IOUS to identify various anatomic structures is shown in Table 1. Intraoperative ultrasound failed to d e m o n s t r a t e the cystic d u c t a n d c o n f l u e n c e in f o u r patients, three o f w h o m h a d adhesions of the o m e n t u m and d u o d e n u m to the liver a n d h e p a t o d u o d e n a l ligament as a result o f severe inflammation. A n o t h e r patient h a d an abe r r a n t posterior b r a n c h o f the bile duct in which the cystic d u c t entered. T h e cystic duct a n d confluence could n o t be d e m o n s t r a t e d by IOUS. T h e c o m m o n bile d u c t was n o t identified in two patients because of i n t e r f e r e n c e by d u o d e n a l gas. Thus, the entire extrahepatic bile duct, cystic duct, and its confluence, excluding ampulla o f Vater, was visualized in 60 o f the 65 patients (92%). T h e c o m m o n hepatic duct, p r o p e r hepatic artery, a n d portal vein were similarly visualized in 64 patients (98%). Anatomic variations o f the bile duct were identified in 12 of the 65 patients. A parallel r u n of the cystic d u c t with the c o m m o n hepatic duct, oi~ a spiral cystic d u c t passing posterior to the c o m m o n hepatic duct was p r e s e n t in 11 patients. A diverticu l u m of the c o m m o n bile d u c t was d e m o n s t r a t e d in 1 patient. Intraoperative ultrasonography detected a low u n i o n o f the hepatic ducts in 1 patient, while IOC could identify an a b e r r a n t posterior b r a n c h of the bile d u c t in which the cystic d u c t entered. Anatomic variations o f the hepatic arteries were identified in 5 patients. Right hepatic artery originating f r o m the superior mesenteric artery was f o u n d in 3, a right hepatic artery ventral to the c o m m o n hepatic d u c t in 1, a n d a low bifurcation of the right hepatic artery in 1.
Intraoperative cholangiography study. Intraoperarive c h o l a n g i o g r a p h y was a t t e m p t e d in 58 o f the 65 patients. The r e m a i n i n g 7 patients were n o t scheduled for cholangiography because o f either their contrast allergies or their overall p o o r physical conditions. Intraoperative c h o l a n g i o g r a p h y was c o m p l e t e d in 54 o f the a t t e m p t e d studies. In the r e m a i n i n g 4 patients, there was failure to cannulate the cystic duct because o f technical difficulties. In 1 patient, there was a suspicion of an anatomic variation of the bile duct, because the cystic d u c t could n o t be identified by IOUS or by laparoscopic inspection. Intraoperative cholangiography t h r o u g h the gallbladder n e c k was attempted, a n d showed the a b e r r a n t posterior b r a n c h of the bile duct. Intraoperative cholangiography was therefore c o m p l e t e d in 54 o f the 58 patients a t t e m p t e d (93%). T h e m e a n duration o f the c h o l a n g i o g r a p h y was 24.4 minutes (95% confidence interval, 22.3-26.9 minutes). The ability of IOC to identify hepatobiliary anatomic detail is d e m o n s t r a t e d in Table 2. T h e entire biliary tree was depicted in 42 o f 54 patients (78%). Anatomic variations o f the bile d u c t were identified in 13 patients, the cystic duct r a n parallel to the c o m m o n hepatic duct, or the spiral cystic duct passed posterior to the c o m m o n hepatic duct in 11 patients; a diverticulum o f the c o m m o n bile d u c t was p r e s e n t in 1; a n d the cystic d u c t e n t e r e d an a b e r r a n t posterior b r a n c h o f the bile d u c t in 1. T h e r e were no complications f r o m IOC d u r i n g any of the laparoscopic cholecystectomies. Comparison between intraoperative ultrasonography and cholangiography in detecting bile duct stones. Bile d u c t stones were identified in six patients by a preoperative e x a m i n a t i o n a n d were r e m o v e d in three o f these patients by endoscopic sphincteroto m y before their laparoscopic cholecystectomies. In the r e m a i n i n g three patients, bile d u c t stones were r e m o v e d laparoscopically by a transcystic c o m m o n bile d u c t exploration. Both examinations d e m o n s t r a t e d a total of seven stones in the extrahepatic bile duct, c o n f i r m e d by intraoperative cholangioscopy in these three patients (Fig. 3). Intraoperative u l t r a s o n o g r a p h y identified a T a b l e 2. A n a t o m i c Sites Visualized by I n t r a o p e r a t i v e C h o l a n g i o g r a p h y in 54 Patients
Intrahepatic bile ducts Extrahepatic bile ducts Hepatic ducts and confluence Common hepatic duct Common bile duct Ampulla of Vater
No. of patients
Percent
48
89
46 48 54 51
85 89 100 94
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FIG 3. A bile duct stone is demonstrated by intraoperative ultrasonography (left). A filling defect (white arrow) in the distal end of the common bile duct is demonstrated by endoscopic retrograde cholangiopancreatography (right). ST, stone; CBD, common bile duct; Pane, pancreas.
3 m m unsuspected stone in the aberrant bile duct of another patient in whom the preoperative examination could not have detected one. Although the cystic duct could not be identified by laparoscopic inspection, and therefore cystic duct cholangiography could not be performed, we attempted IOC via the gallbladder neck, and a stone in an aberrant duct was demonstrated. As it was difficult to explore the c o m m o n bile duct because of the concomitant bile duct anomaly, the stone was small enough to pass into the d u o d e n u m , and therefore the stone was not extracted. Four weeks after the laparoscopic cholecystectomy, the patient's abnormal liver function tests were completely normalized and there have been no biliary symptoms in clinical followup for 25 months. Intraoperative ultrasonography demonstrated many small sharp echoes with acoustic shadows in the anterior branch of the intrahepatic bile ducts in one patient, who underwent extraction of seven large stones by endoscopic sphincterotomy 8 days before a laparoscopic cholecystectomy. This patient has had an uneventful 24-month clinical followup. This finding by IOUS was considered false positive. Small sharp echoes were not demonstrated by IOUS in the other two patients who
underwent endoscopic sphincterotomy for stone removal. Small circular contrast filling defects were demonstrated in two patients by IOC, and IOUS demonstrated no signs of bile duct stones. These patients have had no biliary symptoms and normal liver function tests in clinical followup for the past 26 and 27 months, respectively. These findings by IOC, therefore, were considered false positive. Only one patient in whom neither technique was able to detect bile duct stones actually had small gallbladder stones. This patient developed a recurrent biliary colic with abnormal liver function tests 2 months after a laparoscopic cholecystectomy. Although no stone was identified by postoperative ultrasonography and endoscopic retrograde cholangiopancreatography studies, the cause was related to a r e m n a n t stone that passed into the d u o d e n u m . This is an example of a falsenegative study by IOUS and IOC. The sensitivities, specificities, positive predictive values, negative predictive values, and accuracies for detecting bile duct stones were 80, 98, 80, 98, and 97% by IOUS, and 80, 97, 67, 98, and 95% by IOC, respectively. The time required for IOUS was significantly shorter than for IOC (p < 0.0001).
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Discussion
Routine IOC d u r i n g cholecystectomy has b e e n a controversial issue since the initial work o f Mirizzi (12). Because r o u t i n e IOC is costly, lengthens operative time significantly, a n d has unavoidable freq u e n t false-positive results, m a n y authorities reco m m e n d selective use (1, 3, 4). While several studies have shown the benefit of diagnosing bile d u c t stones preoperatively, a new laparoscopic ultrasonographic device has simplified intraoperative exploration. This probe was recently introd u c e d byJakimowicz a n d others (4, 8, 13, 14). Two r e c e n t reports have d e m o n s t r a t e d that IOUS was comparable to IOC in its ability to detect bile duct stones (10, 11). In addition, our results indicate that IOUS compares favorably with IOC in its capacity to detect bile d u c t stones. This c u r r e n t prospective study d e m o n s t r a t e s that IOUS n o t only has the potential to detect bile d u c t stones, but it c a n also display hepatobiliary a n a t o m y a n d congenital anomalies. Thus, IOUS may aid in intraoperative decision making. T h e sensitivity, specificity, and accuracy rates for d e t e c t i n g bile d u c t stones by IOUS were 80, 98, and 97%, respectively. There-was only o n e falsepositive finding. This particular patient u n d e r w e n t preoperative endoscopic sphincterotomy with a stone removal a n d was d e t e r m i n e d to have stones d u r i n g IOUS. No bile d u c t stones or air bubbles were d e m o n s t r a t e d by IOUS in the o t h e r two patients who u n d e r w e n t stone removal preoperatively by endoscopic sphincterotomy. After preoperative endoscopic sphincterotomy, there may be residual pneumobilia, which w o u l d t h e r e f o r e m a k e IOUS evaluation difficult. T h e r e was one false-negative finding in o u r series. This patient h a d small gallbladder stones that were d e m o n strated by IOUS. Intraoperative cholangiography also failed to d e m o n s t r a t e bile d u c t stones in this patient. Some investigators maintain that multiple small gallbladder stones may be predictive factors for the later d e v e l o p m e n t o f bile duct stones (10, 13). Small stones may easily migrate f r o m the gallbladde r into the cystic a n d c o m m o n bile ducts. T h e r e f o r e , in patients with small gallbladder stones, intraoperative examination to detect conc o m i t a n t bile d u c t stones is mandatory. Otherwise, at IOC, two false-positive findings were determined. O n c e air e n t e r e d the bile d u c t after sphincterotomy, it b e c a m e impossible to discriminate between air a n d stones. Technical skill was n e e d e d to obtain a g o o d c h o l a n g i o g r a m in o r d e r to avoid an inappropriate c h o l e d o c h o t o m y seco n d a r y to a false-positive result.
A l t h o u g h an IOC was c o m p l e t e d in 93% of the a t t e m p t e d studies, the entire extrahepatic bile d u c t was visualized in only 78% o f patients in our series. Traverso and colleagues have r e p o r t e d that the entire biliary tree was visualized in 86% o f their series. T h e y stressed that IOC should always visualize the entire biliary tree regardless o f w h e t h e r the study was p e r f o r m e d on a routine or selective basis (14). O u r study d e m o n s t r a t e d that IOC was able to visualize the c o m m o n hepatic d u c t a n d distal e n d of the bile duct, but the comm o n hepatic d u c t a n d c o n f l u e n c e were not seen in 89 and 85% o f patients, respectively. Thus, approximately 15% incidence of n o t visualizing the c o m m o n hepatic d u c t a n d hepatic ducts conflue n c e will n o t allow the surgeon to detect bile d u c t stones a n d ductal injury. Conversely, the c o m m o n hepatic d u c t and hepatic d u c t c o n f l u e n c e were visualized by IOUS in 100% o f patients studied. T h e limitation of IOUS is that the distal e n d o f the extrahepatic bile d u c t is not well visualized. In addition, the position o f the trocar site, a n d the presence of d u o d e n a l gas may interfere with adequate visualization o f the distal e n d o f the extrahepatic bile duct. No study has yet to d e m o n s t r a t e that IOUS allows the surgeon to avoid bile d u c t injury or aids in the decision to convert to an o p e n cholecystectomy. Intraoperative ultrasonography is useful for detecting the gallbladder n e c k a n d the cystic duct in relation to the c o m m o n bile duct. In addition, IOUS may aid in assessment o f the level o f difficulty of a laparoscopic cholecystectomy. It m i g h t help the surgeon to decide w h e t h e r to convert to an o p e n cholecystectomy, especially in patients with acute cholecystitis. We d e c i d e d to convert a p r o c e d u r e to an o p e n cholecystectomy to prevent bile duct injury in a patient who h a d a gallbladder n e c k that, by IOUS, was closely a d h e r e n t to the c o m m o n hepatic duct. In a n o t h e r patient with acute cholecystitis, IOUS d e m o n s t r a t e d a gallbladder n e c k that was closely a d h e r e n t to the comm o n hepatic duct, a n d this e n a b l e d us to complete the cholecystectomy laparoscopically. Several authors have r e p o r t e d that the efficacy o f IOC could n o t prevent bile d u c t injuries (2, 15, 16). W h e n the cystic duct is mistakenly d e t e c t e d as the extrahepatic bile d u c t a n d incised, a bile d u c t injury has b e e n created, a n d laparotomy is necessary to repair the injury. Needless to say, careful dissection a n d adequate visualization of the i n f u n d i b u l u m , cystic duct, a n d extrahepatic d u c t is essential in o r d e r to prevent bile duct injury. Intraoperative ultrasonography, however, is the preferred m e t h o d for detection o f these structures a n d for determin-
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ing the intraoperative treatment plan. It may aid the decision to convert the p r o c e d u r e to an o p e n cholecystectomy before bile duct injury occurs. T h e m a n a g e m e n t of bile duct stones has bec o m e controversial in the era of the laparoscopic cholecystectomy (17-19). Advanced operative techniques and instrument d e v e l o p m e n t in laparoscopic surgery have resulted in e x p a n d e d treatm e n t options including endoscopic and laparoscopic m a n a g e m e n t of bile duct stones, in addition to the standard o p e n choledochotomy. Intraoperative diagnostic procedures during a laparoscopic cholecystectomy are proving beneficial in bile duct evaluation to d e t e r m i n e treatment plans. Intraoperative ultrasonography is a reliable m e t h o d to detect the presence and position of bile duct stones. O u r results indicate that IOUS is a safe and effective m e t h o d to help surgeons decide w h e t h e r to p r o c e e d with a laparotomy or attempt a laparoscopic bile duct exploration in all patients u n d e r g o i n g a laparoscopic cholecystectomy. If the distal e n d of the extrahepatic bile duct is n o t visualized by IOUS, IOC may be indicated, especially when the diameter of the c o m m o n bile duct exceeds 7 m m (20). This can better define the presence of a ductal stone. During a laparoscopic cholecystectomy, it is most i m p o r t a n t to clearly identify the cystic duct itself before ligation to prevent bile duct injury. Intraoperative ultrasonography was able to help correctly identify the cystic duct and its confluence in o u r series. According to Ascher and colleagues, IOUS with a 12.5 MHz catheter-based ultrasound probe identified the cystic duct in 45% of patients a n d the cystic j u n c t i o n with the c o m m o n hepatic duct in 30% of patients (9). Detectability of the cystic duct and the cystic j u n c t i o n with the comm o n hepatic duct in our series, using the 7.5 MHz lineal array transducer, surpassed their results. A transducer frequency ranging from 5-10 MHz was r e p o r t e d to be favorable for intraoperative exploration of the hepatobiliary system (8, 21). A transducer with a frequency greater than 10 MHz limits the d e p t h of view, and can inhibit the ability to detect the cystic duct or the j u n c t i o n between the cystic and c o m m o n hepatic ducts. This inhibition may be from the variety of junctional sites a m o n g which the cystic and c o m m o n hepatic ducts join. A variety of bile duct anomalies has been r e p o r t e d in subjects p o s t m o r t e m (22-25). To prevent traumatic injuries to the bile duct, detection of bile duct variations during hepatobiliary surgery is of primary importance. O u r results certify that IOUS is useful for detection of the cystic duct entry site. T h e short cystic duct, however, with a low bifurca-
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tion of hepatic ducts, could not be identified by laparoscopic inspection or IOUS. Clear visualization of the gallbladder i n f u n d i b u l u m and the cystic duct is necessary to avoid bile duct injuries in this case. O n e of the advantages that IOUS has in comparison with IOC is its ability to identify blood vessels. In our series, the portal vein could be demonstrated in all cases, and, thus, was a g o o d landmark in identifying anatomic relationships with the nearby c o m m o n bile duct and the hepatic artery. Several authors have reported that anatomic variations of the hepatic arteries frequently exist (24-27). T h e laparoscopic important arterial anomalies may be the low-lying, posterior cystic artery, the "caterpillar h u m p " right hepatic artery, or the accessory right hepatic artery (28). We demonstrated a significant n u m b e r of right hepatic arterial anomalies in 5 of 65 patients (8%) by IOUS. This result is slightly less than that reported in the literature (24-27). Although the hepatic arteries were clearly d e m o n s t r a t e d by IOUS, the course of the cystic artery was depicted in only 46% in our series. T h e c o n t i n u e d i m p r o v e m e n t in the video resolution of the ultrasonographic e q u i p m e n t may enable the cystic artery to be visualized m o r e c o m m o n l y in the future. Several surgeons have r e p o r t e d that routine IOC was not justified because the task is time c o n s u m i n g (3, 4, 14). In o u r series, the time required for IOUS was significantly shorter than for IOC. The m e a n time for IOUS was 9.7 minutes. This is longer than that reported by Rothlin and colleagues (11). A factor that may have led to a p r o l o n g e d examination time in our series was that we attempted to view all of the anatomic relationships of the bile duct, hepatic artery, and portal vein. O n e limitation in our study was that we did n o t use a m o d e r n fluoroscopic system (2). Continued improvements in technique and e q u i p m e n t may further reduce the time n e e d e d for IOC. Intraoperative cholangiography could not, however, be c o m p l e t e d in all patients u n d e r g o i n g a laparoscopic cholecystectomy by skilled surgeons (2). Intraoperative ultrasonography serves as a g o o d screening m e t h o d for detecting the presence of ductal stones or anomalies in all patients u n d e r g o i n g laparoscopic cholecystectomy. O n e of the major limitations of this p r o c e d u r e is that it requires significant technical skill to perform, The transverse plane of the portal structures depicted by IOUS using a 7.5 MHz lineal array transducer resembles the images p r o d u c e d by extracorporeal ultrasonography. We believe that surgeons experi-
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enced in extracorporeal ultrasonography can quickly develop skill with IOUS. In conclusion, IOUS using a 7.5 MHz lineal array transducer is superior to cholangiography in terms of its safety, duration of operative time, and ease of administration in all patients undergoing a laparoscopic cholecystectomy. Intraoperative ultrasonography compares favorably with IOC in exploring bile duct stones and demonstrating hepatobiliary anatomic detail. Finally, IOUS is an effective aid for biliary exploration and guides the surgeon in performing a safe laparoscopic cholecystectomy. References 1. Hauer-Jensen M, Karesen R, Nygaard K, et al. Consequences of routine preoperative cholangiography during cholecystectomy for gallstone disease: a prospective, randomized study. WorldJ Surg 1986;10:996-1002. 2. Berci G, Sackier JM, and Paz-Parlow M. Routine or selected intraoperative cholangiography during laparoscopic cholecystectomy? Am J Surg 1991;161:355-60. 3. Lillemoe KD, Yeo C, Talamini MA, et al. Selective cholangiography: current role in laparoscopic cholecystectomy. Ann Surg 1992;215:669-76. 4. Claire DG, Carr-Locke D, Becker J, and Brooks D. Routine cholangiography is not warranted during laparoscopic cholecystectomy. Arch Surg 1993;128:551-5. 5. Pitt HA. Role of open choledochotomy in the treatment of choledocholithiasis. Am J Surg 1993;165:483-6. 6. Lane RJ, Graham AE, and Coupland MS. Ultrasonic indications to explore the common bile duct. Surgery 1982;91:26874. 7. Sigel B, Machi J, Beitler JC, et al. Comparative accuracy of operative uhrasonography and cholangiography in detecting common duct calculi. Surgery 1983;94:715-20. 8. Jakimowicz JJ. Ultrasound-assisted laparoscopic cholecystectomy: preliminary experience. Dig Surg 1991;8:114-7. 9. Ascher SM, Evans SRT, GoldbergJA, et al. Intraoperative bile duct sonography during laparoscopic cholecystectomy: experience with a 12.5 Mhz catheter-based US probe. Radiology 1992;185:493-6. 10. Grei.gJD, John TG, Mahadavan M, and Garden oJ. Laparoscoplc ultrasonography in the evaluation of the biliary tree during laparoscopic cholecystectomy. Br J Surg 1994;81: 1202-6.
11. Rothlin MA, Schlumpf RS, and Largiader F. Laparoscopic sonography: an alternative to routine intraoperative cholangiography. Arch Surg 1994;129:694-700. 12. Mirizzi PL. Operative cholangiography. Surg Gynecol Obstet 1932;65:702-10. 13. Barkun AN, Barkun JS, Fried GM, et al. Useful predictors of bile duct stones in patients undergoing laparoscopic cholecystectomy. Ann Surg 1994;220:32-9. 14. Traverso LW, Hauptmann EM, and Lynge DC. Routine intraoperative cholangiography and its contribution to the selective cholangiography. Am J Surg 1994;167:464-8. 15. HunterJG. Avoidance of bile duct injury during laparoscopic cholecystectomy. Am J Surg 1991;162:71-6. 16. SackierJM, Berci G, and Phillips E. The role of cholangiography in laparoscopic cholecystectomy. Arch Surg 1991;126: 1021-6. 17. Perissat J, Huibregtse K, Keane FBV, et al. Management of bile duct stones in the era of laparoscopic cholecystectomy. BrJ Surg 1994;81:799-810. 18. Neoptolemos JP, Carr-Locke DL, and Fossard DP. Prospective randomized study of preoperative endoscopic sphincterotomy versus surgery alone for common bile duct stones. Br Med J 1987;294:470-4. 19. Pretelin JB. Laparoscopic approach to common duct pathology. Am J Surg 1993;165:487-91. 20. Jakimowicz JJ. Operative and technology section: review: intraoperative ultrasonography during minimal access surgery. J R Coll Surg Edinb 1993;38:231-8. 2!. MachiJ, and Sigel B. Intraoperative ultrasonography. Radiol Clin North Am 1992;30:1085-103. 22. Kune GE. The influence of structure and function in the surgery of the bilialY tract. Ann R Coll Surg Engl 1970;47: 78-91. 23. Hayes MA, Goldberg IS, and Bishop CC. The developmental basis for bile duct anomalies. Surg Gynecol Obstet 1985;107: 447-56. 24. Cole WH. Congenital anomalies of tile bile ducts and adjacent blood vessels. Surg Gynecol Obstet 1948;87:111-2. 25. Eisendrath DN. Anomalies of the bile ducts and blood vessels as the cause of accidents in biliary surgery. JAMA 1918;71: 864-7. 26. HiattJR, Gabby J, and Busulttil RW. Surgical anatomy of the hepatic arteries in 1,000 cases. Ann Surg 1994;220:50-2. 27. Benson EA, and Page RE. A practical reappraisal of the anatomy of the extrahepatic bile ducts and arteries. BrJ Surg 1976;63:853-60. 28. Scott CEH, and Hall TJ. Variant arterial anatomy in laparoscopic cholecystectomy. Am J Surg 1992;163:590-2.
were 80, 98, 80, 98, and 97% by IOUS, and 80, 97, 67, 98, and 95% by IOC, respectively.
the functional utility of intraoperative ultrasonography (IOUS) and cholangiography (IOC) during a laparoscopic cholecystectomy for the treatment of gallstone disease.
Conclusions: Intraoperative ultrasonography is superior to cholangiography with respect to its safety, shorter examination period, and ease of administration in all patients. In addition, IOUS is also better for identifying subtle anatomic detail. Intraoperative ultrasonography compares favorably with IOC in terms of utility in exploring bile ducts for stones. Intraoperative ultrasonography is an effective procedure for biliary exploration during a laparoscopic cholecystectomy. (J Am Coil Surg 1997;185:274-282. © 1997 by the American College of Surgeons)
Study Design:A prospective study comparing IOUS and IOC was carried out in 65 patients. Intraoperative ultrasonography was conducted first using a 7.5-MHz linear array probe. After IOUS, IOC was then conducted in all patients. The respective usefulness of IOUS and IOC in the identification of gallstones, detection of hepatobiliary structures, and demonstration of congenital anomalies was then compared. Results: Intraoperative ultrasonography was successful in all 65 patients, and IOC was successful only in 54. The time required for IOUS was significantly shorter (p < 0.0001) than for IOC. Intraoperative ultrasonography imaged the hepatic ducts and their confluence, the common hepatic duct, the common bile duct, and the ampulla of Vater in 97, 100, 97, and 51% of cases, respectively. Intraoperative cholangiography, on the other hand, depicted these structures in 85, 89, 100, and 94% of cases, respectively. Intraoperative ultrasonography demonstrated the cystic duct and its confluence in 94% of cases. Biliary anomalies were identified by IOUS in 12 patients and by IOC in 13. Intraoperative ultrasonography could detect the hilar vascular structures in most patients and visualized anomalies of the hepatic arteries in 5 patients. In this series, 5 patients had choledocholithiasis. The sensitivities, speciflcities, positive and negative predictive values, and accuracies in identifying these bile duct stones ReceivedJanuary 13, 1997;AcceptedMarch 24, 1997. From the *Departmentof Surgery,NiigataUniversitySchoolof Medicine, and the tDepartment of Surgery,The Nippon Dental University, Niigata,Japan. This work was supported in part by a Grant-in-Aid for Scientific Research (C) fromthe Ministryof Education,Science,and Cultureof Japan, accountno. 07671373. Correspondence address: TetsuyaOhtani, MD, Departmentof Surgee/, Niigata UniversitySchool of Medicine, 1-757Asahimachi-dori, Niigata, 951,Japan. © 1997 by the AmericanCollegeof Surgeons Published by ElsevierScienceInc.
MD,*
Intraoperative c h o l a n g i o g r a p h y (IOC) for gallstone disease d u r i n g an o p e n cholecystectomy has b e e n very useful in detecting u n s u s p e c t e d bile d u c t stones a n d anomalies of the biliary system. This p r o c e d u r e , however, has disadvantages including a high percentage of false-positive cholangiograms a n d a lengthy operative time a n d high cost (1). In the era of the laparoscopic cholecystectomy, r o u t i n e or selected IOC has thus b e c o m e controversial (2-4). T h e prevalence of bile d u c t stones, however, must n o t be disregarded, as they are f o u n d in 7-20% of patients with c o n c o m i t a n t gallbladder stones (5). Intraoperative screening for choledocholithiasis is therefore crucial, because this enables the surgeons to use several t r e a t m e n t options laparoscopically at the time of surgery, a n d as a result, avoid unnecessary postoperative intervention. T h e clinical use o f real-time B m o d e ultrasonography for gallstone disease was first described by Lane a n d colleagues (6), and Sigel and colleagues (7). They have reported that intraoperative ultrasonography (IOUS) was a reliable m e t h o d for detecting bile duct stones during an open cholecystectomy and demonstrated several advantages of IOUS compared with IOC (6, 7). The use of IOUS during a laparoscopic cholecystectomy was first reported by Jakimowicz (8), and recently some authors have de-
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FIG l. Transverse scans of linear array ultrasonography on the hepatoduodenal ligament through the epigastric port. (A) The ultrasonography demonstrates the cystic duct and common hepatic duct. (B) The cystic duct is clearly seen entering the common bile duct. (C) The intrapancreatic part of the common bile duct is visualized. (D) Ampulla of Vater and d u o d e n u m are demonstrated. CD, cystic duct; CHD, common hepatic duct; CBD, common bile duct; Panc, pancreas; DU, duodenum; Am, ampulla of Vater; PV, portal vein; IVC, inferior vena cava.
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scribed more specifically the operative technique and clinical indications (9-11). In our study, we have prospectively evaluated the effectiveness of IOUS and IOC for the detection of choledocholithiasis and hepatobiliary anatomic structures and anomaries during a laparoscopic cholecystectomy. Me~o~
Patient population. From J u n e 1993 to September 1994, 68 consecutive patients with suspected gallstone disease were referred to our institution. A laparoscopic cholecystectomy was a t t e m p t e d in all patients. Preoperative assessment consisted of obtaining a complete history; physical examination; transabdominal ultrasonography; liver function tests including measurements of serum bilirubin, asparate aminotransferase, alanine aminotransferase, and alkaline phosphatase; and a serum amylase level. Every patient's clinical course was carefully followed and recorded. Technique of laparoscopic cholecystectomy and intraoperative studies. Laparoscopic cholecystectomy was p e r f o r m e d using a standard four-puncture technique. After establishing p n e u m o p e r i t o n e u m , a 10 m m umbilical trocar was inserted into the peritoneal cavity. While carefully inspecting the abdominal cavity with the laparoscope, a 10 m m trocar in the epigastrium, a 5 m m trocar in the right midclavicular line, a n d a 5 m m trocar in the anterior axillar line were inserted. Before u l t r a s o n o g r a p h i c e x a m i n a t i o n , sterile saline was instilled into the peritoneal cavity over the hepat o d u o d e n a l ligament in order to provide an appropriate acoustic window. If structures were adh e r e n t to the gallbladder, they were dissected first. The ultrasonographic probe was then i n t r o d u c e d t h r o u g h the epigastric p o r t u n d e r direct visualization, with the laparoscope functioning t h r o u g h t h e umbilical port. T h e gallbladder wall and its contents were visualized t h r o u g h the liver parenchyma using the ultrasonographic probe. W h e n the probe was moved on the liver medially, the anterior and posterior branches of the portal pedicle and its j u n c t i o n were demonstrated. T h e probe was then positioned to the lateral surface of the liver to the right of the h e p a t o d u o d e n a l ligament. W h e n the probe was dragged down laterally to the right of the h e p a t o d u o d e n a l ligament and rotated clockwise, the transverse planes of the extrahepatic bile duct, p r o p e r hepatic artery, and portal vein were visualized in their entirety (Fig. 1). T h e ultrasonographic probe was subsequently introd u c e d u n d e r direct visualization into the umbilical port, with the laparoscope functioning in the epi-
FIG 2. Longitudinal scans of linear array ultrasonography through the umbilical port. The ultrasound scan clearly demonstrates the cysticduct entering the common bile duct. The right hepatic artery is seen between the common hepatic duct and the portal vein. CD, cystic duct; CHD, common hepatic duct; PV, portal vein; RHA, right hepatic artery; IVC, inferior vena cava.
gastric port. The longitudinal planes of the bile duct, portal vein, and inferior vena cava were then d e m o n s t r a t e d through the liver parenchyma and by direct contact with the h e p a t o d u o d e n a l ligam e n t (Fig. 2). T h e transverse plane of the right hepatic artery, lying between the extrahepatic bile duct a n d portal vein, was d e m o n s t r a t e d in the hepatic hilum using this technique (Fig. 2). Intraoperative ultrasonographic imaging was perf o r m e d using a 7.5 MHz lineal array transducer of the Aloka laparoscopic ultrasonographic probe (UST-5522-7.5, Aloka Co Ltd., Tokyo, Japan). An ultrasound scanner, the Aloka SSD 1200 (Aloka Co Ltd., Tokyo, Japan), was also used in this investigation. After completing the IOUS, the triangle of Callot was then dissected with cephalad traction on the gallbladder fundus and lateral traction on the infundibulum. The cystic duct was identified and freed entirely and then secured by a clip placed close to the gallbladder. Intraoperative cholangiography was carried o u t with the Olsen
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cholangiography fixation clamp (Karl Storz Endoscopy, Culver City, CA). The clamp was inserted through either epigastric port or the port located in the right anterior axillar line. We routinely infused 5-10 mL of contrast material (Urografin, Schering Corp., Osaka, Japan) in order to demonstrate duodenal flow of the contrast material. The duodenal papilla was visualized using fluoroscopy (Model TVM-128 = KN, Toshiba Corp., Kawasaki, Japan). Additional contrast material (5-10 mL) was then infused through the catheter, and x-ray films were obtained in order to detect choledocholithiasis. A cholecystectomy was performed only after dissection of the cystic duct and artery was complete, and after the intraoperative studies described above. The cholecystectomy was completed using electrocautery dissection, and the resected gallbladder was removed through the epigastric trocar.
Comparative studies between intraoperative ultrasonogTaphy and cholangiography. A prospective comparative study was undertaken to evaluate IOUS and IOC in identifying bile duct stones, hepatobiliary anatomic details, and congenital anomalies. The durations of these two examinations were compared in order to evaluate their feasibility. Intraoperative ultrasound was evaluated in terms of its accuracy in demonstrating anatomic details. The anatomic sites that were evaluated with IOUS included the following: the hepatic ducts and confluence, the c o m m o n hepatic duct, the c o m m o n bile duct, the cystic duct, the cystic d u c t confluence, the ampulla of Vater, the proper hepatic artery, the right hepatic artery, the cystic artery, and the portal vein (Figs. 1 and 2). Arteries were distinguished from other structures by the presence of pulsation. Detailed descriptive records were kept on patients who had bile duct stones or anomalies of the biliary system and hepatic arteries. A sharp echo with an acoustic shadow in the bile duct was defined as positive for a bile duct stone. The time required for IOUS was measured from the initial introduction of the probe to its removal from the trocar. Intraoperative cholangiography visualizing the biliary tree with contrast material was then carried out. The intrabiliary sites visualized by cholangiography included the following: the intrahepatic bile ducts, the hepatic ducts and confluence, the c o m m o n hepatic duct, the c o m m o n bile duct, and the ampulla of Vater. Specific points of interest during cholangiography were the presence or absence of filling defects and the identification of bile duct anomalies. A contrast-filling defect in the bile duct was defined as positive for a bile duct stone. The time required
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for IOC was measured from the initial clipping of the gallbladder site to the biliary ductal display on the film illuminator. Laparoscopic cholecystect0my was performed by three of the authors (TO, CK, and KK). The preoperative transabdominal ultrasonography, IOUS, and IOC were carried out by one surgeon (TO) experienced in ultrasonography. The two groups were compared statistically using the Student's unpaired t-test. Sensitivity, specificity, predictive values, and accuracy for both groups were then calculated. Results
Patient characteristics. A laparoscopic cholecystectomy was attempted in all 68 patients r e f e r r e d to our institution, but conversion to an open procedure was necessary in 2 patients after examination by IOUS. In one patient with severe acute cholecystitis, uncontrolled bleeding of a liver bed laceration occurred during the dissection of Callot triangle and resulted in conversion to an open cholecystectomy. In another patient, an incarcerated gallstone in the gallbladder neck provoked hydrops, and the gallbladder neck was closely adh e r e n t to the c o m m o n hepatic duct by IOUS. We therefore decided to proceed with an open cholecystectomy in order to prevent bile duct injury. The operation was completed laparoscopically in the remaining 66 patients (97%). In 1 of the 66 patients, a preoperative diagnosis of cholelithiasis was made, but only gallbladder polyps without stones .were identified by IOUS a n d later confirmed histologically. The 65 patients who had confirmed gallstones were entered into a prospective comparative study. Twenty-four patients were men and 41 patients were women. The average age of the group was 53.3 years (range, 20-85 years). Bile duct injury, bile leak, and vessel injury were observed neither during nor after laparoscopic cholecystectomy in these 65 patients. Previous abdominal operations had been performed in 26 of the 65 patients (39%); an upper abdominal incision was performed in 2 patients, and a lower abdominal incision in 25. The mean followup time after surgery was 23 months (range, 15-30 months). Intraoperative ultrasonographic study. Intraoperarive ultrasonography was tolerated in all 65 patients during the laparoscopic cholecystectomy. Before IOUS, lysis of the adhesions around the gallbladder was necessary in 17 patients, 2 patients seconda~y to previous abdominal surgery, and 15 secondary to inflammation related to cholecystitis.
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T a b l e 1. A n a t o m i c Sites Visualized by I n t r a o p e r a t i v e U l t r a s o n o g r a p h y in 65 P a t i e n t s
Extrahepatic bile ducts Hepatic ducts and confluence Common hepatic duct Common bile duct Cystic duct and confluence Ampulla of Vater Vessels Portal vein Proper hepatic artery Right hepatic artery Cystic artery
No. of patients
Percent
63 65 63 61 33
97 100 97 94 51
65 64 63 30
100 98 97 46
T h e m e a n e x a m i n a t i o n d u r a t i o n was 9.7 minutes (95% c o n f i d e n c e interval, 9.0-10.4 minutes). In one patient with acute cholecystitis, although the IOUS d e m o n s t r a t e d a gallbladder neck closely adh e r e n t to the c o m m o n hepatic duct, a laparoscopic cholecystectomy was c o m p l e t e d with careful dissection between the gallbladder n e c k a n d the c o m m o n hepatic duct. T h e ability o f IOUS to identify various anatomic structures is shown in Table 1. Intraoperative ultrasound failed to d e m o n s t r a t e the cystic d u c t a n d c o n f l u e n c e in f o u r patients, three o f w h o m h a d adhesions of the o m e n t u m and d u o d e n u m to the liver a n d h e p a t o d u o d e n a l ligament as a result o f severe inflammation. A n o t h e r patient h a d an abe r r a n t posterior b r a n c h o f the bile duct in which the cystic d u c t entered. T h e cystic duct a n d confluence could n o t be d e m o n s t r a t e d by IOUS. T h e c o m m o n bile d u c t was n o t identified in two patients because of i n t e r f e r e n c e by d u o d e n a l gas. Thus, the entire extrahepatic bile duct, cystic duct, and its confluence, excluding ampulla o f Vater, was visualized in 60 o f the 65 patients (92%). T h e c o m m o n hepatic duct, p r o p e r hepatic artery, a n d portal vein were similarly visualized in 64 patients (98%). Anatomic variations o f the bile duct were identified in 12 of the 65 patients. A parallel r u n of the cystic d u c t with the c o m m o n hepatic duct, oi~ a spiral cystic d u c t passing posterior to the c o m m o n hepatic duct was p r e s e n t in 11 patients. A diverticu l u m of the c o m m o n bile d u c t was d e m o n s t r a t e d in 1 patient. Intraoperative ultrasonography detected a low u n i o n o f the hepatic ducts in 1 patient, while IOC could identify an a b e r r a n t posterior b r a n c h of the bile d u c t in which the cystic d u c t entered. Anatomic variations o f the hepatic arteries were identified in 5 patients. Right hepatic artery originating f r o m the superior mesenteric artery was f o u n d in 3, a right hepatic artery ventral to the c o m m o n hepatic d u c t in 1, a n d a low bifurcation of the right hepatic artery in 1.
Intraoperative cholangiography study. Intraoperarive c h o l a n g i o g r a p h y was a t t e m p t e d in 58 o f the 65 patients. The r e m a i n i n g 7 patients were n o t scheduled for cholangiography because o f either their contrast allergies or their overall p o o r physical conditions. Intraoperative c h o l a n g i o g r a p h y was c o m p l e t e d in 54 o f the a t t e m p t e d studies. In the r e m a i n i n g 4 patients, there was failure to cannulate the cystic duct because o f technical difficulties. In 1 patient, there was a suspicion of an anatomic variation of the bile duct, because the cystic d u c t could n o t be identified by IOUS or by laparoscopic inspection. Intraoperative cholangiography t h r o u g h the gallbladder n e c k was attempted, a n d showed the a b e r r a n t posterior b r a n c h of the bile duct. Intraoperative cholangiography was therefore c o m p l e t e d in 54 o f the 58 patients a t t e m p t e d (93%). T h e m e a n duration o f the c h o l a n g i o g r a p h y was 24.4 minutes (95% confidence interval, 22.3-26.9 minutes). The ability of IOC to identify hepatobiliary anatomic detail is d e m o n s t r a t e d in Table 2. T h e entire biliary tree was depicted in 42 o f 54 patients (78%). Anatomic variations o f the bile d u c t were identified in 13 patients, the cystic duct r a n parallel to the c o m m o n hepatic duct, or the spiral cystic duct passed posterior to the c o m m o n hepatic duct in 11 patients; a diverticulum o f the c o m m o n bile d u c t was p r e s e n t in 1; a n d the cystic d u c t e n t e r e d an a b e r r a n t posterior b r a n c h o f the bile d u c t in 1. T h e r e were no complications f r o m IOC d u r i n g any of the laparoscopic cholecystectomies. Comparison between intraoperative ultrasonography and cholangiography in detecting bile duct stones. Bile d u c t stones were identified in six patients by a preoperative e x a m i n a t i o n a n d were r e m o v e d in three o f these patients by endoscopic sphincteroto m y before their laparoscopic cholecystectomies. In the r e m a i n i n g three patients, bile d u c t stones were r e m o v e d laparoscopically by a transcystic c o m m o n bile d u c t exploration. Both examinations d e m o n s t r a t e d a total of seven stones in the extrahepatic bile duct, c o n f i r m e d by intraoperative cholangioscopy in these three patients (Fig. 3). Intraoperative u l t r a s o n o g r a p h y identified a T a b l e 2. A n a t o m i c Sites Visualized by I n t r a o p e r a t i v e C h o l a n g i o g r a p h y in 54 Patients
Intrahepatic bile ducts Extrahepatic bile ducts Hepatic ducts and confluence Common hepatic duct Common bile duct Ampulla of Vater
No. of patients
Percent
48
89
46 48 54 51
85 89 100 94
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FIG 3. A bile duct stone is demonstrated by intraoperative ultrasonography (left). A filling defect (white arrow) in the distal end of the common bile duct is demonstrated by endoscopic retrograde cholangiopancreatography (right). ST, stone; CBD, common bile duct; Pane, pancreas.
3 m m unsuspected stone in the aberrant bile duct of another patient in whom the preoperative examination could not have detected one. Although the cystic duct could not be identified by laparoscopic inspection, and therefore cystic duct cholangiography could not be performed, we attempted IOC via the gallbladder neck, and a stone in an aberrant duct was demonstrated. As it was difficult to explore the c o m m o n bile duct because of the concomitant bile duct anomaly, the stone was small enough to pass into the d u o d e n u m , and therefore the stone was not extracted. Four weeks after the laparoscopic cholecystectomy, the patient's abnormal liver function tests were completely normalized and there have been no biliary symptoms in clinical followup for 25 months. Intraoperative ultrasonography demonstrated many small sharp echoes with acoustic shadows in the anterior branch of the intrahepatic bile ducts in one patient, who underwent extraction of seven large stones by endoscopic sphincterotomy 8 days before a laparoscopic cholecystectomy. This patient has had an uneventful 24-month clinical followup. This finding by IOUS was considered false positive. Small sharp echoes were not demonstrated by IOUS in the other two patients who
underwent endoscopic sphincterotomy for stone removal. Small circular contrast filling defects were demonstrated in two patients by IOC, and IOUS demonstrated no signs of bile duct stones. These patients have had no biliary symptoms and normal liver function tests in clinical followup for the past 26 and 27 months, respectively. These findings by IOC, therefore, were considered false positive. Only one patient in whom neither technique was able to detect bile duct stones actually had small gallbladder stones. This patient developed a recurrent biliary colic with abnormal liver function tests 2 months after a laparoscopic cholecystectomy. Although no stone was identified by postoperative ultrasonography and endoscopic retrograde cholangiopancreatography studies, the cause was related to a r e m n a n t stone that passed into the d u o d e n u m . This is an example of a falsenegative study by IOUS and IOC. The sensitivities, specificities, positive predictive values, negative predictive values, and accuracies for detecting bile duct stones were 80, 98, 80, 98, and 97% by IOUS, and 80, 97, 67, 98, and 95% by IOC, respectively. The time required for IOUS was significantly shorter than for IOC (p < 0.0001).
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Discussion
Routine IOC d u r i n g cholecystectomy has b e e n a controversial issue since the initial work o f Mirizzi (12). Because r o u t i n e IOC is costly, lengthens operative time significantly, a n d has unavoidable freq u e n t false-positive results, m a n y authorities reco m m e n d selective use (1, 3, 4). While several studies have shown the benefit of diagnosing bile d u c t stones preoperatively, a new laparoscopic ultrasonographic device has simplified intraoperative exploration. This probe was recently introd u c e d byJakimowicz a n d others (4, 8, 13, 14). Two r e c e n t reports have d e m o n s t r a t e d that IOUS was comparable to IOC in its ability to detect bile duct stones (10, 11). In addition, our results indicate that IOUS compares favorably with IOC in its capacity to detect bile d u c t stones. This c u r r e n t prospective study d e m o n s t r a t e s that IOUS n o t only has the potential to detect bile d u c t stones, but it c a n also display hepatobiliary a n a t o m y a n d congenital anomalies. Thus, IOUS may aid in intraoperative decision making. T h e sensitivity, specificity, and accuracy rates for d e t e c t i n g bile d u c t stones by IOUS were 80, 98, and 97%, respectively. There-was only o n e falsepositive finding. This particular patient u n d e r w e n t preoperative endoscopic sphincterotomy with a stone removal a n d was d e t e r m i n e d to have stones d u r i n g IOUS. No bile d u c t stones or air bubbles were d e m o n s t r a t e d by IOUS in the o t h e r two patients who u n d e r w e n t stone removal preoperatively by endoscopic sphincterotomy. After preoperative endoscopic sphincterotomy, there may be residual pneumobilia, which w o u l d t h e r e f o r e m a k e IOUS evaluation difficult. T h e r e was one false-negative finding in o u r series. This patient h a d small gallbladder stones that were d e m o n strated by IOUS. Intraoperative cholangiography also failed to d e m o n s t r a t e bile d u c t stones in this patient. Some investigators maintain that multiple small gallbladder stones may be predictive factors for the later d e v e l o p m e n t o f bile duct stones (10, 13). Small stones may easily migrate f r o m the gallbladde r into the cystic a n d c o m m o n bile ducts. T h e r e f o r e , in patients with small gallbladder stones, intraoperative examination to detect conc o m i t a n t bile d u c t stones is mandatory. Otherwise, at IOC, two false-positive findings were determined. O n c e air e n t e r e d the bile d u c t after sphincterotomy, it b e c a m e impossible to discriminate between air a n d stones. Technical skill was n e e d e d to obtain a g o o d c h o l a n g i o g r a m in o r d e r to avoid an inappropriate c h o l e d o c h o t o m y seco n d a r y to a false-positive result.
A l t h o u g h an IOC was c o m p l e t e d in 93% of the a t t e m p t e d studies, the entire extrahepatic bile d u c t was visualized in only 78% o f patients in our series. Traverso and colleagues have r e p o r t e d that the entire biliary tree was visualized in 86% o f their series. T h e y stressed that IOC should always visualize the entire biliary tree regardless o f w h e t h e r the study was p e r f o r m e d on a routine or selective basis (14). O u r study d e m o n s t r a t e d that IOC was able to visualize the c o m m o n hepatic d u c t a n d distal e n d of the bile duct, but the comm o n hepatic d u c t a n d c o n f l u e n c e were not seen in 89 and 85% o f patients, respectively. Thus, approximately 15% incidence of n o t visualizing the c o m m o n hepatic d u c t a n d hepatic ducts conflue n c e will n o t allow the surgeon to detect bile d u c t stones a n d ductal injury. Conversely, the c o m m o n hepatic d u c t and hepatic d u c t c o n f l u e n c e were visualized by IOUS in 100% o f patients studied. T h e limitation of IOUS is that the distal e n d o f the extrahepatic bile d u c t is not well visualized. In addition, the position o f the trocar site, a n d the presence of d u o d e n a l gas may interfere with adequate visualization o f the distal e n d o f the extrahepatic bile duct. No study has yet to d e m o n s t r a t e that IOUS allows the surgeon to avoid bile d u c t injury or aids in the decision to convert to an o p e n cholecystectomy. Intraoperative ultrasonography is useful for detecting the gallbladder n e c k a n d the cystic duct in relation to the c o m m o n bile duct. In addition, IOUS may aid in assessment o f the level o f difficulty of a laparoscopic cholecystectomy. It m i g h t help the surgeon to decide w h e t h e r to convert to an o p e n cholecystectomy, especially in patients with acute cholecystitis. We d e c i d e d to convert a p r o c e d u r e to an o p e n cholecystectomy to prevent bile duct injury in a patient who h a d a gallbladder n e c k that, by IOUS, was closely a d h e r e n t to the c o m m o n hepatic duct. In a n o t h e r patient with acute cholecystitis, IOUS d e m o n s t r a t e d a gallbladder n e c k that was closely a d h e r e n t to the comm o n hepatic duct, a n d this e n a b l e d us to complete the cholecystectomy laparoscopically. Several authors have r e p o r t e d that the efficacy o f IOC could n o t prevent bile d u c t injuries (2, 15, 16). W h e n the cystic duct is mistakenly d e t e c t e d as the extrahepatic bile d u c t a n d incised, a bile d u c t injury has b e e n created, a n d laparotomy is necessary to repair the injury. Needless to say, careful dissection a n d adequate visualization of the i n f u n d i b u l u m , cystic duct, a n d extrahepatic d u c t is essential in o r d e r to prevent bile duct injury. Intraoperative ultrasonography, however, is the preferred m e t h o d for detection o f these structures a n d for determin-
Ohtani et al
COMPARISON OF ULTRASONOGRAPHY AND C H O L A N G I O G R A P H Y
ing the intraoperative treatment plan. It may aid the decision to convert the p r o c e d u r e to an o p e n cholecystectomy before bile duct injury occurs. T h e m a n a g e m e n t of bile duct stones has bec o m e controversial in the era of the laparoscopic cholecystectomy (17-19). Advanced operative techniques and instrument d e v e l o p m e n t in laparoscopic surgery have resulted in e x p a n d e d treatm e n t options including endoscopic and laparoscopic m a n a g e m e n t of bile duct stones, in addition to the standard o p e n choledochotomy. Intraoperative diagnostic procedures during a laparoscopic cholecystectomy are proving beneficial in bile duct evaluation to d e t e r m i n e treatment plans. Intraoperative ultrasonography is a reliable m e t h o d to detect the presence and position of bile duct stones. O u r results indicate that IOUS is a safe and effective m e t h o d to help surgeons decide w h e t h e r to p r o c e e d with a laparotomy or attempt a laparoscopic bile duct exploration in all patients u n d e r g o i n g a laparoscopic cholecystectomy. If the distal e n d of the extrahepatic bile duct is n o t visualized by IOUS, IOC may be indicated, especially when the diameter of the c o m m o n bile duct exceeds 7 m m (20). This can better define the presence of a ductal stone. During a laparoscopic cholecystectomy, it is most i m p o r t a n t to clearly identify the cystic duct itself before ligation to prevent bile duct injury. Intraoperative ultrasonography was able to help correctly identify the cystic duct and its confluence in o u r series. According to Ascher and colleagues, IOUS with a 12.5 MHz catheter-based ultrasound probe identified the cystic duct in 45% of patients a n d the cystic j u n c t i o n with the c o m m o n hepatic duct in 30% of patients (9). Detectability of the cystic duct and the cystic j u n c t i o n with the comm o n hepatic duct in our series, using the 7.5 MHz lineal array transducer, surpassed their results. A transducer frequency ranging from 5-10 MHz was r e p o r t e d to be favorable for intraoperative exploration of the hepatobiliary system (8, 21). A transducer with a frequency greater than 10 MHz limits the d e p t h of view, and can inhibit the ability to detect the cystic duct or the j u n c t i o n between the cystic and c o m m o n hepatic ducts. This inhibition may be from the variety of junctional sites a m o n g which the cystic and c o m m o n hepatic ducts join. A variety of bile duct anomalies has been r e p o r t e d in subjects p o s t m o r t e m (22-25). To prevent traumatic injuries to the bile duct, detection of bile duct variations during hepatobiliary surgery is of primary importance. O u r results certify that IOUS is useful for detection of the cystic duct entry site. T h e short cystic duct, however, with a low bifurca-
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tion of hepatic ducts, could not be identified by laparoscopic inspection or IOUS. Clear visualization of the gallbladder i n f u n d i b u l u m and the cystic duct is necessary to avoid bile duct injuries in this case. O n e of the advantages that IOUS has in comparison with IOC is its ability to identify blood vessels. In our series, the portal vein could be demonstrated in all cases, and, thus, was a g o o d landmark in identifying anatomic relationships with the nearby c o m m o n bile duct and the hepatic artery. Several authors have reported that anatomic variations of the hepatic arteries frequently exist (24-27). T h e laparoscopic important arterial anomalies may be the low-lying, posterior cystic artery, the "caterpillar h u m p " right hepatic artery, or the accessory right hepatic artery (28). We demonstrated a significant n u m b e r of right hepatic arterial anomalies in 5 of 65 patients (8%) by IOUS. This result is slightly less than that reported in the literature (24-27). Although the hepatic arteries were clearly d e m o n s t r a t e d by IOUS, the course of the cystic artery was depicted in only 46% in our series. T h e c o n t i n u e d i m p r o v e m e n t in the video resolution of the ultrasonographic e q u i p m e n t may enable the cystic artery to be visualized m o r e c o m m o n l y in the future. Several surgeons have r e p o r t e d that routine IOC was not justified because the task is time c o n s u m i n g (3, 4, 14). In o u r series, the time required for IOUS was significantly shorter than for IOC. The m e a n time for IOUS was 9.7 minutes. This is longer than that reported by Rothlin and colleagues (11). A factor that may have led to a p r o l o n g e d examination time in our series was that we attempted to view all of the anatomic relationships of the bile duct, hepatic artery, and portal vein. O n e limitation in our study was that we did n o t use a m o d e r n fluoroscopic system (2). Continued improvements in technique and e q u i p m e n t may further reduce the time n e e d e d for IOC. Intraoperative cholangiography could not, however, be c o m p l e t e d in all patients u n d e r g o i n g a laparoscopic cholecystectomy by skilled surgeons (2). Intraoperative ultrasonography serves as a g o o d screening m e t h o d for detecting the presence of ductal stones or anomalies in all patients u n d e r g o i n g laparoscopic cholecystectomy. O n e of the major limitations of this p r o c e d u r e is that it requires significant technical skill to perform, The transverse plane of the portal structures depicted by IOUS using a 7.5 MHz lineal array transducer resembles the images p r o d u c e d by extracorporeal ultrasonography. We believe that surgeons experi-
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enced in extracorporeal ultrasonography can quickly develop skill with IOUS. In conclusion, IOUS using a 7.5 MHz lineal array transducer is superior to cholangiography in terms of its safety, duration of operative time, and ease of administration in all patients undergoing a laparoscopic cholecystectomy. Intraoperative ultrasonography compares favorably with IOC in exploring bile duct stones and demonstrating hepatobiliary anatomic detail. Finally, IOUS is an effective aid for biliary exploration and guides the surgeon in performing a safe laparoscopic cholecystectomy. References 1. Hauer-Jensen M, Karesen R, Nygaard K, et al. Consequences of routine preoperative cholangiography during cholecystectomy for gallstone disease: a prospective, randomized study. WorldJ Surg 1986;10:996-1002. 2. Berci G, Sackier JM, and Paz-Parlow M. Routine or selected intraoperative cholangiography during laparoscopic cholecystectomy? Am J Surg 1991;161:355-60. 3. Lillemoe KD, Yeo C, Talamini MA, et al. Selective cholangiography: current role in laparoscopic cholecystectomy. Ann Surg 1992;215:669-76. 4. Claire DG, Carr-Locke D, Becker J, and Brooks D. Routine cholangiography is not warranted during laparoscopic cholecystectomy. Arch Surg 1993;128:551-5. 5. Pitt HA. Role of open choledochotomy in the treatment of choledocholithiasis. Am J Surg 1993;165:483-6. 6. Lane RJ, Graham AE, and Coupland MS. Ultrasonic indications to explore the common bile duct. Surgery 1982;91:26874. 7. Sigel B, Machi J, Beitler JC, et al. Comparative accuracy of operative uhrasonography and cholangiography in detecting common duct calculi. Surgery 1983;94:715-20. 8. Jakimowicz JJ. Ultrasound-assisted laparoscopic cholecystectomy: preliminary experience. Dig Surg 1991;8:114-7. 9. Ascher SM, Evans SRT, GoldbergJA, et al. Intraoperative bile duct sonography during laparoscopic cholecystectomy: experience with a 12.5 Mhz catheter-based US probe. Radiology 1992;185:493-6. 10. Grei.gJD, John TG, Mahadavan M, and Garden oJ. Laparoscoplc ultrasonography in the evaluation of the biliary tree during laparoscopic cholecystectomy. Br J Surg 1994;81: 1202-6.
11. Rothlin MA, Schlumpf RS, and Largiader F. Laparoscopic sonography: an alternative to routine intraoperative cholangiography. Arch Surg 1994;129:694-700. 12. Mirizzi PL. Operative cholangiography. Surg Gynecol Obstet 1932;65:702-10. 13. Barkun AN, Barkun JS, Fried GM, et al. Useful predictors of bile duct stones in patients undergoing laparoscopic cholecystectomy. Ann Surg 1994;220:32-9. 14. Traverso LW, Hauptmann EM, and Lynge DC. Routine intraoperative cholangiography and its contribution to the selective cholangiography. Am J Surg 1994;167:464-8. 15. HunterJG. Avoidance of bile duct injury during laparoscopic cholecystectomy. Am J Surg 1991;162:71-6. 16. SackierJM, Berci G, and Phillips E. The role of cholangiography in laparoscopic cholecystectomy. Arch Surg 1991;126: 1021-6. 17. Perissat J, Huibregtse K, Keane FBV, et al. Management of bile duct stones in the era of laparoscopic cholecystectomy. BrJ Surg 1994;81:799-810. 18. Neoptolemos JP, Carr-Locke DL, and Fossard DP. Prospective randomized study of preoperative endoscopic sphincterotomy versus surgery alone for common bile duct stones. Br Med J 1987;294:470-4. 19. Pretelin JB. Laparoscopic approach to common duct pathology. Am J Surg 1993;165:487-91. 20. Jakimowicz JJ. Operative and technology section: review: intraoperative ultrasonography during minimal access surgery. J R Coll Surg Edinb 1993;38:231-8. 2!. MachiJ, and Sigel B. Intraoperative ultrasonography. Radiol Clin North Am 1992;30:1085-103. 22. Kune GE. The influence of structure and function in the surgery of the bilialY tract. Ann R Coll Surg Engl 1970;47: 78-91. 23. Hayes MA, Goldberg IS, and Bishop CC. The developmental basis for bile duct anomalies. Surg Gynecol Obstet 1985;107: 447-56. 24. Cole WH. Congenital anomalies of tile bile ducts and adjacent blood vessels. Surg Gynecol Obstet 1948;87:111-2. 25. Eisendrath DN. Anomalies of the bile ducts and blood vessels as the cause of accidents in biliary surgery. JAMA 1918;71: 864-7. 26. HiattJR, Gabby J, and Busulttil RW. Surgical anatomy of the hepatic arteries in 1,000 cases. Ann Surg 1994;220:50-2. 27. Benson EA, and Page RE. A practical reappraisal of the anatomy of the extrahepatic bile ducts and arteries. BrJ Surg 1976;63:853-60. 28. Scott CEH, and Hall TJ. Variant arterial anatomy in laparoscopic cholecystectomy. Am J Surg 1992;163:590-2.