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AJR 2004; 183:1567-1572
© American Roentgen Ray Society

Value of MR Cholangiography in Patients with Iatrogenic Bile Duct Injury After Cholecystectomy

Alfonso Ragozzino1, Rosaria De Ritis1, Alessandro Mosca2, Vittorio Iaccarino3 and Massimo Imbriaco1,3

1 Department of Radiology, Cardarelli Hospital, Via Pansini 5, Via Manzoni 214/0, Naples 80123, Italy.
2 Department of Gastroenterology, Cardarelli Hospital, Naples 80123, Italy.
3 Department of Radiology, University Federico II, Naples, Italy.

Received February 26, 2004; accepted after revision April 30, 2004.

 
Address correspondence to M. Imbriaco (mimbriaco{at}hotmail.com).


Abstract
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 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
OBJECTIVE. Our aim was to determine the diagnostic role of MR cholangiography in the evaluation of iatrogenic bile duct injuries after cholecystectomy.

SUBJECTS AND METHODS. Nineteen patients (14 women and five men; mean age, 47 years; age range, 24–75 years) with suspected bile duct injury as a result of laparoscopic cholecystectomy (17 patients) and open cholecystectomy (two patients) underwent MR cholangiography. MR images were evaluated for bile duct discontinuity, presence or absence of biliary dilation, stricture, excision injury, free fluid, and collections. Bile duct excision and stricture were classified according to the Bismuth classification. Final diagnosis was made on the basis of findings at surgery in 15 patients, on percutaneous transhepatic cholangiography (PTC) in one patient, and on endoscopic retrograde cholangiography (ERC) and at clinical follow-up until hospital discharge in the remaining three patients.

RESULTS. In 16 patients, injury of the bile duct was observed. Two patients had Bismuth type I injury; one patient, type II injury; 11 patients, type III injury; and one patient each, type IV and V injuries. Three patients showed findings suggestive of leakage from the cystic duct remnant, which were confirmed on ERC.

CONCLUSION. MR cholangiography is an accurate diagnostic technique in the identification of postoperative bile duct injuries. This technique allows exploration above and below the level of obstruction, a resource provided by neither ERC nor PTC, and allows the accurate classification of these injuries, which is essential for treatment planning.


Introduction
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 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
Iatrogenic injury of the biliary tract after cholecystectomy is a complex problem for both surgeons and patients. The incidence of these lesions has increased from 0.3% to 1.2% in hospitals with extensive experience with cholecystectomy [1]. In particular, incidence varies from 0.1% to 0.5% for open cholecystectomy and from 0% to 1.2% for laparoscopic cholecystectomy [2, 3]. Bile duct injuries vary in their severity and longterm consequences. Most of these lesions result from misinterpretation of either normal or variant anatomy [4]. In the most severe form, the common bile duct is mistaken for the cystic duct and is ligated and divided, with or without ligation of the common hepatic duct. Damage to the bile duct may also take the form of a laceration, occlusion without tissue loss, or thermal injury from electrocautery [5].

The initial treatment of these patients depends on the type of injury and the time of its recognition. Therefore, it is essential to determine the exact nature of the injury and define the anatomy of the proximal biliary tree, which in turn, determines the strategy for biliary reconstruction and affects the prognosis. Percutaneous transhepatic cholangiography (PTC) and endoscopic retrograde cholangiography (ERC) have traditionally been used for the evaluation of bile duct injuries. MR cholangiography is a relatively new application of abdominal MRI that enables visualization of the biliary tree without the need for contrast material and thus without any known side effects.

Only a few articles have been published in the literature on the role of MR cholangiography in patients with suspected biliary injuries [6–8]. The aim of this prospective study was to evaluate the role of MR cholangiography in the assessment of iatrogenic bile duct injuries after cholecystectomy.


Subjects and Methods
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 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
From April 1999 to December 2003, nineteen patients (14 women and five men; mean age, 47 years; age range, 24–75 years) with clinical findings suggestive of postoperative bile duct injury were prospectively studied with MR cholangiography after laparoscopic cholecystectomy in 17 patients and open cholecystectomy in two patients. Among all the patients who were referred for MR cholangiography at our institution with suspected bile duct injury after cholecystectomy, the final study group included only patients for whom direct cholangiography or final surgical correlation was available.

Details of the study were explained by a physician, and informed consent was obtained from all patients. Clinical symptoms included the presence of persistent right-upper-quadrant abdominal pain, jaundice, fever, and abnormal findings on liver function tests. ERC was performed in six patients; one patient underwent PTC; in two patients, T-tube cholangiography was also performed; and four patients underwent CT. All MR cholangiograms were evaluated by two expert abdominal imaging radiologists who were aware of each patient's clinical history and serology findings. Final diagnosis was made on the basis of findings at surgery in 15 patients, on PTC findings in one patient, and on ERC findings and at clinical follow-up until hospital discharge in the remaining three patients.

MR cholangiography studies were performed on a 1.5-T scanner (Eclipse, Marconi). A body coil was used in all patients. Breath-hold axial fast spin-echo T2-weighted images were obtained using the following parameters: TR/effective TE, 18,000/84; matrix, 256 x 256; acquisition, 1; scanning time, 18 sec; and slice thickness, 5 mm. Four 30- to 50-mm-thick sections were then acquired in oblique coronal planes along the course of the bile duct (as seen in the axial images), using a field of view of 35–38 cm. The scanning time for each section was less than 8 sec. Subsequently, 5-mm-thick no-gap breath-hold fat-suppressed coronal images (scanning time, 16 sec) were obtained. Two-dimensional and 3D images were finally generated from the coronal source images using a maximum-intensity-projection algorithm and multiplanar reformatting techniques.

The total scanning time in all patients ranged between 20 and 25 min. In one case, axial and coronal volumetric 3D spoiled gradient-echo images of the biliary tract (TR/TE, 5/2; flip angle, 40°; matrix, 220 x 128; partitions for a slice thickness of 2.5 mm, 26–28) were obtained after the IV administration of mangafodipir trisodium (Teslascan, Nycomed Amersham) at a standard dose of 5 mmol/kg (0.1 mL/kg; maximum dose, 15 mL) via a slow injection over 3–5 min. Scanning was initiated 15 min after the injection, and two or three sets of volumetric 3D axial and coronal images were obtained every 5–10 min. Subsequently, maximum-intensity-projection reconstructions of the 3D image sets were obtained.

MR images were considered of good diagnostic quality in all patients, and no examination was canceled because of lack of patient compliance. MR images were evaluated for bile duct discontinuity, presence or absence of biliary dilation, stricture, excision injury, free fluid, and collections. Biliary excision injury was defined as complete lack of visualization of a bile duct segment on reconstructed images and on the source images with secondary bile duct obstruction. Biliary injuries were classified according to the Bismuth classification [9]. Bismuth type I injury is a traumatic injury of the main bile duct occurring more than 2 cm distal from the biliary confluence. A type II injury is located less than 2 cm from the biliary bifurcation. A type III injury involves the common hepatic duct but leaves the confluence intact. A type IV injury completely or partially involves the biliary confluence. A type V injury involves the right variant segmental branch with or without involvement of the main duct. In all cases, MR cholangiography was performed from 2 to 16 days after the surgical procedure.


Results
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 Abstract
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 Subjects and Methods
 Results
Discussion
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Injury of the bile duct was observed in 16 patients. Of these, two patients had Bismuth type I injuries seen on MR cholangiography as a stricture at the level of the common bile duct more than 2 cm from the biliary confluence (Fig. 1); one patient had Bismuth type II injury; and 11 patients had Bismuth type III injuries, showing destruction of the common hepatic duct, leaving the biliary confluence intact, with associated presence of intrahepatic bile duct dilation. An example of Bismuth type III injury is shown in Figure 2. One patient had a Bismuth type IV injury, with a 4-cm-long discontinuity involving the bifurcation (Fig. 3A, 3B), and one patient had a Bismuth type V injury, with involvement of the right variant segmental branch and the common hepatic duct (Fig. 4A, 4B). In three patients, MR cholangiography showed an intact biliary tree with small collections adjacent to the cystic duct remnant and evidence of free fluid.



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  		Fig. 1. —39-year-old man with Bismuth type I injury [9] 1 week after laparoscopic cholecystectomy. MR cholangiogram shows stricture (arrow) at level of common hepatic duct more than 2 cm from biliary confluence. Patient was treated with hepaticojejunostomy.

 


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  		Fig. 2. —41-year-old woman with Bismuth type III injury [9] 8 days after laparoscopic cholecystectomy. MR cholangiogram shows stricture (arrow) at level of common hepatic duct, leaving biliary confluence intact. Patient was treated with hepaticojejunostomy.

 


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  		Fig. 3A. —63-year-old man with Bismuth type IV injury [9] 10 days after laparoscopic cholecystectomy. MR cholangiogram (A) and maximum-intensity-projection image (B) show stricture at level of common hepatic duct with extension and partial destruction of biliary confluence (arrows). Patient was treated with hepaticojejunostomy.

 


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  		Fig. 3B. —63-year-old man with Bismuth type IV injury [9] 10 days after laparoscopic cholecystectomy. MR cholangiogram (A) and maximum-intensity-projection image (B) show stricture at level of common hepatic duct with extension and partial destruction of biliary confluence (arrows). Patient was treated with hepaticojejunostomy.

 


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  		Fig. 4A. —54-year-old woman with Bismuth type V injury [9] 12 days after laparoscopic cholecystectomy. T-tube cholangiogram shows only distal part of biliary tree with no visualization of common hepatic duct or of intrahepatic biliary tracts.

 


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  		Fig. 4B. —54-year-old woman with Bismuth type V injury [9] 12 days after laparoscopic cholecystectomy. MR cholangiogram shows stricture at level of right posterolateral duct (short arrow) with associated involvement of common hepatic duct (long arrow). Patient was treated with hepaticojejunostomy.

 

Cystic duct leak was suggested as the diagnosis on the basis of these findings. ERC confirmed the presence of bile leaks. In one patient with a bile leak, axial and coronal volumetric 3D spoiled gradient-echo images obtained after the IV administration of mangafodipir trisodium confirmed free extravasation of contrast agent from the cystic duct remnant, compatible with a leak (Fig. 5A, 5B). In the other two patients with a bile leak observed on MR cholangiography, mangafodipir trisodium was not used to confirm this diagnosis because of the patients' refusals. All these patients were treated with percutaneous drainage.



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  		Fig. 5A. —75-year-old woman with bile leak from cystic duct remnant 1 week after laparoscopic cholecystectomy. Coronal fat-suppressed T2-weighted image shows small collection adjacent to cystic duct remnant (arrow).

 


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  		Fig. 5B. —75-year-old woman with bile leak from cystic duct remnant 1 week after laparoscopic cholecystectomy. Coronal volumetric maximum-intensity-projection mangafodipir trisodium–enhanced image confirms extravasation of contrast material into subhepatic space (arrow). Patient was treated with percutaneous drainage.

 

In the remaining three patients who also underwent ERC, MR cholangiography accurately revealed the entire biliary system both proximal and distal to the amputated or stenotic site, whereas ERC showed only the distal common bile duct stump and a complete cutoff at that point. In four patients, CT revealed nonspecific or equivocal findings that were only complementary without any impact on the final diagnosis. Table 1 shows patients' characteristics and summarizes the types of biliary injuries with the corresponding treatments.


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  		TABLE 1 Clinical Characteristics, Type of Surgery, Type of Biliary Injury, and Treatment in 19 Patients

 


Discussion
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
The results of this study show that MR cholangiography is an accurate diagnostic technique in the identification of postoperative bile duct injuries. This technique allows exploration above and below the level of the obstruction, a resource provided by neither ERC nor PTC, and may permit accurate classification of bile duct injuries, which is essential for treatment planning.

Injuries to the bile duct are a serious problem, potentially life-threatening. They are an important cause of morbidity, prolonged hospitalization, and high costs for the health care system [10, 11]. The immediate cause of biliary injury can be related to misidentification of the biliary structures; in particular, misidentifications may occur when there is an aberrant right duct or when the bile duct is mistaken for the cystic duct. Frequent causes of bile duct injury might also be the following technical problems: failure to securely occlude the cystic duct, a plane of dissection of the gallbladder too deep off the liver bed, and thermal injuries to the bile duct. Biliary injury during open cholecystectomy has been well recognized and described in the literature [12–15].

The incidence of iatrogenic biliary tract injury in open cholecystectomy is widely accepted to be between 0.1% and 0.5%, whereas the incidence of injuries during laparoscopic cholecystectomy is variably reported as ranging from from 0% to 1.2% and can be as high as 4% in laparoscopic cholecystectomy for acute cholecystitis. Soon after its introduction, laparoscopic cholecystectomy was associated with a high rate of complications compared with the open approach. Early reports of injuries of the common bile duct injury due to laparoscopic cholecystectomy were two to 15 times greater than those identified with open cholecystectomy [16, 17].

A case series of 1,518 laparoscopic cholecystectomies suggested that the high rate of injury was mainly related to early experience with this technique, the so-called learning curve effect [18]. As the procedure has become increasingly common, surgeons have tended to cite a rate of injury of 1:300. However, despite the broad experience of surgeons with laparoscopic cholecystectomy during the past decade, rates of injury as high as 1.4% have recently been reported [19]. The impact of a major common bile duct injury is staggering to both the patient and the health care system. Major common biliary injury is associated with an 11% case fatality [20] and almost always requires a technically demanding expensive operative reconstruction of the biliary tree [21]. In a series of 46 bile duct injuries during laparoscopic cholecystectomy, Carroll et al. [22] have shown that 80% of these injuries were not detected at the initial surgery, with an average delay in the diagnosis of 10 days. These authors concluded that factors that predispose to lawsuits include treatment failures because the injury was not immediately recognized and complications that resulted from delayed diagnosis and misinterpretation of abnormal cholangiograms. Therefore, these injuries have a significant health and economic impact [23].

The early treatment of these patients should focus on accurate assessment of the injury, control of infection (cholangitis or abscess), and drainage of the bile. There is no standard approach to the early diagnosis of bile duct injury in the available reports [6, 7]. A number of algorithms have been proposed for the diagnosis and management of biliary injuries [24, 25]. The five main techniques traditionally used are the following: CT, Doppler sonography, hepatobiliary scintigraphy, ERC, and PTC. Contrast-enhanced CT and Doppler sonography are the conventional initial studies. These techniques allow definition of the level of injury, identification of fluid collections or the presence of ascites, and detection of the possibility of vascular damage and lobar atrophy. Furthermore, the main role of these investigations, coupled with percutaneous aspiration, is to establish the presence of bile in the peritoneal cavity and eventually to drain it.

Hepatobiliary scintigraphy is good for the detection of bile leakage; however, this technique lacks the anatomic detail needed for preoperative planning. The main purpose of investigation should be to establish the diagnosis with the least risk of morbidity and the lowest cost. In particular, the main roles of the more invasive procedures, such as ERC and PTC, are to provide exact anatomic diagnosis and to treat the injury by decompressing the biliary tree or dilating it. In general, PTC is superior to ERC in the case of biliary excision in providing critical anatomic details of the proximal biliary tree. Evaluation by ERC in the case of complete stenosis is limited by the fact that it shows only the lower end of the obstruction and fails to delineate the proximal biliary tract [26]. Nevertheless, these procedures are invasive and have the potential for serious complications such as acute pancreatitis, hemorrhage, infection, perforation, aspiration, and adverse reaction to contrast media or premedication [27].

In agreement with previous studies [6–8], we confirm that MR cholangiography is an accurate noninvasive technique for assessing bile duct injuries after surgery. In particular, this technique allows exact definition of the level and the length of the biliary injury that is essential for preoperative planning. In addition, MR cholangiography allows detection of the presence of subhepatic abscesses or collections and shows the site of bile leakage. In comparison to ERC and PTC, MR cholangiography offers the advantages of being rapid and noninvasive and can be performed emergently, providing good images of the biliary tree with accurate and precise delineation of the injury. Furthermore, MR cholangiography can also delineate the anatomic variants, such as low and right-sided insertion of the cystic duct, a parallel course of the cystic duct with the hepatic duct, and the presence of an aberrant right hepatic duct [28].

Several authors have recently proposed the possible use of contrast-enhanced MR cholangiography after the IV administration of mangafodipir trisodium in the detection and localization of bile duct leaks in patients who have undergone cholecystectomy [29–32]. Mangafodipir trisodium is an MRI hepatobiliary contrast agent that consists of manganese bound to dipyridoxyl diphosphate, a vitamin B6 analog. It can provide useful dynamic and functional information similar to that obtained on hepatic scintigraphy and anatomic information similar to that found on conventional contrast-enhanced cholangiography. After the IV administration of mangafodipir trisodium, manganese accumulates within the liver and is primarily excreted via bile [29–32]. In agreement with findings in one patient in our series, these authors found that MR cholangiography performed after the IV injection of mangafodipir trisodium allowed correct identification of the site of bile leak. Therefore, the use of contrast-enhanced MR cholangiography with IV mangafodipir trisodium should be recommended in patients thought to have bile duct leaks after cholecystectomy, providing accurate anatomic and, in particular, functional information that allows prompt diagnosis and treatment of bile leaks.

The main limitation of MR cholangiography is that it is only diagnostic and has no therapeutic potential; subsequent biliary stents must still be placed by ERC or PTC before any surgical attempt to repair the bile ducts. ERC has been advocated as a potential useful first-line investigation in patients with major common bile duct injuries [32]. However, although useful in the management of biliary injuries, this technique combined with sphincterotomy has a complication rate that ranges from 7% to 11%, with a mortality rate of 1.5% [33]. More recent publications state a complication rate of 5–10% in ERC with sphincterotomy [34]. Therefore, we believe that in the near future, MR cholangiography might represent the first-line noninvasive diagnostic test in patients with suspected bile duct injuries after surgery, allowing correct treatment of these patients by surgical, endoscopic, or percutaneous procedures.

A potential limitation of this study is the small size of our study group. Additional multiinstitutional trials using larger patient populations are therefore needed to validate our findings.

In conclusion, MR cholangiography may definitely replace ERC or PTC as an accurate diagnostic tool in patients with bile duct injuries after surgery, allowing the correct classification of these injuries, which is essential for treatment planning.


Acknowledgments
 
We thank Graciana Diez-Roux for critically reviewing our manuscript, Ciro Anatrella and Vincenzo Braun for assisting as technologists, and Carmela Imparato for editing the manuscript.


References
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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