Abstract
Abstract
Purpose:
Bile duct injuries (BDIs) are more frequent during laparoscopic cholecystectomy (LC). Several BDI classifications are reported, but none encompasses anatomy of damage and vascular injury (A), timing of detection (To), and mechanism of damage (M). Aim was to apply the ATOM classification to a series of patients referred for BDI management after LC.
Methods:
From 2008 to 2016, 26 patients (16 males and 10 females, median age 63 years, range 34–82 years) with BDIs were observed. Fifteen patients were managed by percutaneous transhepatic cholangiography (PTC)+endoscopic retrograde cholangiopancreatography (ERCP); five and six underwent PTC and ERCP alone, respectively. Median overall follow-up duration was 34 months. Three patients died from sepsis.
Results:
Out of 26 patients, 20 presented with main bile duct and six with nonmain bile duct injuries. Using the ATOM classification, every aspect of the BDI in every case was included, unlike with other classifications (Neuhaus, Lau, Strasberg, Bergman, and Hanover).
Conclusions:
The all-inclusive European Association for Endoscopic Surgery (EAES) classification contains objective data and emphasizes the underlying mechanisms of damage, which is relevant for prevention. It also integrates vascular injury, necessary for ultimate management, and timing of discovery, which has diagnostic implications. The management complexity of these patients requires specialized referral centers.
Introduction
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Because of the complexity of the phenomenon and of its treatment, several classifications have been proposed in an attempt to categorize the type of injury and to standardize the treatment strategy.6–8,11–14,18–27 For each classification, however, one or more relevant features of BDI necessary to thoroughly describe its complexity are lacking. 6 For this reason, the European Association for Endoscopic Surgery (EAES) proposed an all-inclusive BDI nominal classification system (ATOM), which includes the anatomy of damage and occurrence of vascular injury (A), the timing of detection (To), and the mechanism of damage (M). 6
The aim of this study was to apply the ATOM classification to a series of septic patients who were referred to our Hospital for interventional radiological and endoscopic management of a BDI that occurred during LC. For the purpose of this study, each BDI was classified according to the ATOM classification and also according to five of the most popular classifications (Neuhaus, Lau, Strasberg, Bergman, and Hanover13,14,22–24), comparing the ability of each classification to represent all the features of each BDI.
Materials and Methods
From June 2008 to February 2016, 26 patients (16 males and 10 females, median age 63 years, range 34–82) were referred to Policlinico Umberto I, Sapienza University of Rome, Italy, for management of a BDI after LC.
Based on the postoperative clinical and radiologic chart review, each patient's BDI was retrospectively classified according to the ATOM classification. 6 Main bile duct (MBD) injuries were classified according to ATOM classification, as follows: (1) low, main BDI >2 cm distal to inferior border of superior hepatic confluence; (2) middle, main BDI <2 cm distal to inferior border of superior hepatic confluence; (3) high, main BDI involving the superior hepatic confluence with left–right communication preserved; (4) high, main BDI involving the superior hepatic confluence with left–right communication interrupted; (5) left or right hepatic duct injuries without injury to the superior confluence; and (6) injury of isolated segmental hepatic duct. 6 According to the ATOM classification nonmain bile duct (NMBD) injuries include the cystic duct and the accessory ducts (hepatic bed, subhepatic, Luschka). 6 LS was defined as the length in centimeters between two divisions of the same duct, creating a segment that was mistakenly removed or destroyed at surgery. 6 The ATOM classification allows to classify if a Division (D) or an Occlusion (O) occurred, if the ductal injury was complete (c) or partial (p) and if a concurrent vascular injury had occurred (VBI+ or vasculobiliary injury). 6 Time of detection of the injury (early intraoperative [Ei], early postoperative [Ep], or late [L]) and mechanism of injury (mechanical [Me] or energy driven [ED]) are also included. 6
BDIs were also classified according to five of the most popular classifications (Neuhaus, Lau, Strasberg, Bergman, and Hanover13,14,22–24), and a comparison between them was made.
Twenty-five LC had been performed in another hospital and only 1 patient in Policlinico Umberto I, but in a different department from that of the authors of this study. Due to the presence of sepsis, all patients were managed either by percutaneous transhepatic cholangiography (PTC) or by endoscopic retrograde cholangiopancreatography (ERCP) alone, or by a combined radiologic and endoscopic rendezvous procedure (PTC+ERCP), as previously described. 28
Results
At admission, nearly two-thirds (17 of 26) of patients presented with a leak while 9 patients (34.6%) presented with jaundice, attesting to the open or occluded nature of the injury, respectively (Table 1). All patients presented with signs of sepsis, as measured by white blood cell (WBC) counts and C-reactive protein (CRP) levels (mean WBC 17.008 ± 2.613 × 10 3 /μL, mean CRP 105,115.38 ± 53,694.94 μg/L). Using the ATOM classification, it was possible to classify all types and every aspect of each BDI (Table 2). Twenty patients presented with MBD injuries. Of these, 17 had proximal injuries (MBD3 [n = 6], MBD4 [n = 6], MBD5 [n = 4], MBD6 [n = 1]), and three had more distal injuries (MBD1 [n = 1] and MBD2 [n = 2]). The injury was complete in 19 out of 20 cases; Dc and Oc occurred in 10 and 9 patients, respectively. Dp was observed only in 1 patient. LS occurred in 8 patients, and it extended for 1 cm or more in 7 of these cases (mean 2.1 cm, range 0.2–6 cm). A VBI+ was observed by computed tomography scan in 2 patients, including a ruptured pseudoaneurysm at the origin of the cystic artery, while the other involved bleeding from a marginal vessel (MV). Timing of detection was Ei in 1 patient, Ep in 17 patients, and L in 2 patients. The mechanism of injury in these patients was Me in just over two-thirds (14 of 26), ED in five, and both mechanical and energy driven in one (Tables 2 and 3).
ERCP, endoscopic retrograde cholangiopancreatography; PTC, percutaneous transhepatic cholangiography.
In bold italic, the type of lesions of the patients who eventually died from sepsis.
Dc, division complete; Dp, division partial; ED, energy driven; Ei, early intraoperative; Ep, early postoperative; ERCP, endoscopic retrograde cholangiopancreatography; L, late; LS, loss of substance; MBD, main bile duct; Me, mechanical; MV, marginal vessel; NMBD, nonmain bile duct; Oc, occlusion complete; PTC, percutaneous transhepatic cholangiography; RHA, right hepatic artery; VBI, vasculobiliary injury.
ED, energy driven; Ei, early intraoperative; Ep, early postoperative; L, late; LS, loss of substance; MBD, main bile duct; Me, mechanical; MV, marginal vessel; NMBD, nonmain bile duct (Luschka or other accessory duct); VBI, vasculobiliary injury.
Six patients presented with NMBD injuries. Of these, five were cystic duct leaks from accidental dislodgement of metal clips, and one was a complete division of a Luschka duct from the hepatic bed. None of these injuries was associated with LS or with vascular involvement (VBI−). All NMBD injuries were mechanical, timing of detection was Ep in 5 patients and L in one (Tables 2 and 3).
As shown in Table 4, it was impossible to completely classify these lesions with five of the most commonly used classifications (Neuhaus, Lau, Strasberg, Bergman, and Hanover13,14,22–24) because one or more relevant details of the injuries are missing from the classification. In the Neuhaus and Bergman classifications, details such as anatomic level, time of detection, LS, type of VBI, and mechanism of injury are missing.13,20 In the Lau classification, features such as timing of detection, mechanism of injury, LS, and type of lesion cannot be included. 14 In the Strasberg classification, details such as LS, VBI, type of lesion, and time of detection of the lesions are missing. 19 Also, in the Hanover classification, important details such as VBI, time of detection, mechanism of injury, LS, and anatomical level of the injury are missing (Table 4). 24
In bold italic, the type of lesions of the patients who eventually died from sepsis.
Dc, complete division; Dp, partial division; ED, energy driven; Ei, early intraoperative; Ep, early postoperative; ERCP, endoscopic retrograde cholangiopancreatography; L, late; LS, loss of substance; MBD, main bile duct; Me, mechanical; MV, marginal vessel; n.c., not classified; NMBD, nonmain bile duct; Oc, complete occlusion; PTC, percutaneous transhepatic cholangiography; RHA, right hepatic artery; VBI, vasculobiliary injury. Missing details: Al, anatomic level; LS, loss of substance; M, mechanism; ToD, time of detection; Tol, type of lesion; VBI, vasculobiliary injury.
As per the management of these patients, 15 underwent a combined rendezvous PTC+ERCP procedure (Tables 1 and 2), followed in 1 case by emergency open surgery for brisk bleeding from a ruptured pseudoaneurysm at the origin of the cystic artery that had developed during LC, which was controlled by surgical ligation of the right hepatic artery. The second VBI was managed by MV radiological embolization (Table 2). Five patients were managed by PTC alone, with a mean number of procedures of 4 (range 1–15) (Tables 1 and 2). Six patients underwent ERCP alone for NMBD leaks (Tables 1 and 2). Of these, 5 patients with cystic duct leaks were managed with biliary stent positioning after endoscopic sphincterotomy (ES), and 1 patient who presented with a Luschka duct leak was treated by ES alone. A percutaneous abdominal drainage was positioned in 1 of these cases to drain a subhepatic abscess.
Median follow-up duration was 34 months (range 2–88). No strictures were observed in this series. Three patients died from sepsis. The remaining 23 patients are presently alive without sequelae (Table 1).
Discussion
In this retrospective study, each BDI was more accurately and completely described according to the ATOM classification, including, in each case, the level of the lesion on the biliary tree, the type of injury, the extent of the LS, the occurrence of a VBI, when present, the timing of detection, and the mechanism of injury. Being all-inclusive, this classification method is the most complete classification available today, and it allows all BDI classified with the other systems to be compared between themselves. 29
The previously published classifications of BDIs had several positive features but also weaknesses.6–8,11–14,18–27 The Bismuth classification was based on the distance of the injury (stricture) from the main biliary confluence, and it was aimed at defining the length of common hepatic duct that would be available for surgical hepaticojejunostomy repair. 18 NMBD injuries, leaks, and VBIs were not included.11,18 In Strasberg's classification, partial division of the right or left hepatic duct was not included, as well as the possible presence and extent of LS and of vasculobiliary involvement. 19 In Strasberg's Type E, only occlusion but not division may be classified. 19 According to Lau's classification, features such as the anatomical level of the injury, the extent of tissue loss, the mechanism of injury, and the occurrence of a concomitant vascular injury cannot be classified. 14 The other classifications found in the literature also have shortcomings, such as lack or incompleteness of anatomical characteristics (McMahon, Siewert, Bergman, Csendes, Stewart-Way, Sandha, Kapoor, and Cannon),7,12,20–23,25,27 type and extent of injuries (McMahon, Siewert, Neuhaus, Bergman, Csendes, Stewart-Way, Sandha, Bektas, and Cannon),7,12,13,20–24,27 VBI, timing of detection, and mechanism of injury (McMahon, Connor-Garden, Bismuth, Siewert, Neuhaus, Lau, Strasberg, Bergman, Csendes, Stewart-Way, Sandha, Bektas, Kapoor, Li, and Cannon)7,8,11–14,18–27 (Table 4), making it impossible to compare BDI between themselves. Thus, the ATOM classification seems appropriate, not only to better describe the complexity of the clinical picture in each case but also to provide a baseline, all-inclusive classification to allow for comparisons.
The choice between a surgical or radiological and endoscopic treatment for the management of iatrogenic BDIs is still debated.8,10,28,30,31 According to Connor, a surgical hepaticojejunostomy is to be preferred, but this is not always possible due to the presence of a septic abdominal environment and to the small diameter of the bile ducts at the time the injury occurs. 8 If a segment of the biliary tree or biliary stricture is present, adequate upstream dilatation is required to perform a wide enough hepaticojejunostomy (1–3 cm) that takes ∼3 months to occur. 8 In case of delayed detection of the injury and in the absence of early peritoneal drainage, severe intraperitoneal inflammation and sepsis can occur. 8 Surgical repair in these conditions is associated with dismal postoperative results. 8 Biliary tract injuries are often associated with vascular injuries of the right or left hepatic artery or of the MVs of the bile ducts. 1 The policy that recommends to wait before performing the repair takes into consideration also the time required for the development of a collateral circulation, because ischemia is a common cause of stricture and restricture. 30 Mortality rates after surgical repair are reported to be low but do exist, and postoperative morbidity ranges between 9.5% and 42.9%. 30 Furthermore, the incidence of stricture and restricture of the biliodigestive anastomosis ranges between 6% and 32%, at a mean follow-up of 6 years (range 4–9.5 years).30,32 To avoid strictures, Lillemoe 10 suggested to perform an end-to-side anastomosis protected by a transanastomotic stent, which is left in place for at least 9 months, and report a 9% postoperative stricture rate. 10
The combined radiologic/endoscopic approach is less invasive. It is reported to be associated with good results,28,30 and it may be the only reasonable option in the septic patient. Since an anastomosis is not performed, there is no need to wait for biliary tree dilatation or for development of collateral circulation to occur.28,30 A comparison of endoscopic with surgical treatment showed that early complications were more common in the surgical group and late complications from stent occlusion were more common in the endoscopic group. 33 Long-term results were similar in both groups, with a 17% stricture rate at a mean follow-up of 4.1 years after endoscopy and 3.5 years after surgery. 33 However, whatever treatment strategy is adopted, clinical practice guidelines recommend that patients with such complex injuries should be referred to specialized units for their management. 1 In the present series, the choice for a combined radiologic and/or endoscopic approach stemmed from the fact that all patients in this series presented with severe, moderate, or mild septic conditions and that our hospital is a referral center for nonoperative management of benign biliary lesions.28,34,35 The long-standing interventional radiological and endoscopic experience in this type of management provided the basis to use this nonoperative approach even in case of more complex lesions. Limitations of this approach include the long delay required to obtain healing of the biliary lesion and a 15%–20% radiological/endoscopic reintervention rate which, however, does not preclude the possibility of a delayed surgical revision. This, however, was not required in the present series.
The diagnosis of a major BDI was intraoperative only in 1 case (Tables 2–4), and its management was correctly deferred by the primary surgeon. In fact, the EAES guidelines recommend that a major BDI recognized intraoperatively should be managed in a referral center and not in the hospital where the injury occurred, if the expertise to manage such complex scenario is missing in the index center. 1
MBD tangential injuries are the easiest ones to be managed endoscopically. In cases in which the lesion causes a LS yielding to impaired continuity of the duct, its repair is more challenging. In these cases, which may include either complete transection or complete occlusion, the major issue is to restore bile duct continuity by means of endoscopic–radiological rendezvous. Endoscopic management is preferred in case of NMBD repair, and a percutaneous approach should be considered only in case of endoscopic failure.
The cystic artery pseudoaneurysm was not suitable for endovascular approach due to unfavorable anatomy: the lesion was too tortuous and too close to a bifurcation to permit covered stenting. Coiling was not attempted due to the presence of a large neck and because the etiopathogenesis at onset (bile leak) would have predisposed to pseudoaneurysm enlargement and recurrence.
Limitations of the study were its retrospective, not prospective, nature and the limited sample size.
To the best of the authors' knowledge, this is the first clinical study, in which the ATOM classification of BDIs was applied and all the relevant features of the injury were identified in each case. Although the classification may appear complex, ATOM is the only classification that allows true comparisons with the others because it is all-inclusive, and there are no missing details (as in the case with others) (Table 4). 36 It includes objective data and not subjective terms, such as major, minor, peripheral, central, significant, and insignificant. It allows comparisons of mechanisms and timing of BDI between the other classifications. Last but not least, it emphasizes the underlying mechanism that led to the injury, the most relevant aspect for didactic purposes aiming at prevention. The time is now ripe for this classification to be prospectively validated in larger patient series. 37
Footnotes
Author Disclosure Statement
Dr. Andrea Balla, Dr. Silvia Quaresima, Dr. Mario Corona, Dr. Pierleone Lucatelli, Prof. Fausto Fiocca, Prof. Massimo Rossi, Prof. Mario Bezzi, Prof. Carlo Catalano, Dr. Filippo M. Salvatori, Prof. Abe Fingerhut, and Prof. Alessandro M. Paganini report no conflicts of interest. The authors alone are responsible for the content and writing of the article.
