Abstract
Bile duct injury (BDI) remains a critical complication following cholecystectomy. Prevention, early recognition, and appropriate management can significantly improve patient outcomes. In this chapter, we will discuss the current review of the surgical management of BDI, including prevention techniques during the cholecystectomy, intra-operative diagnosis of the injury, early evaluation and imaging, importance and challenges of the referrals to a hepatobiliary center, types and classification of biliary injuries, biliary drainage, and interventional procedures bridging to definitive repair, timing of surgical repair-early versus late, surgical repair techniques, evaluation and management of combined vasculo-biliary injury.
Keywords
- prevention
- intra-operative diagnosis
- early referral
- cholangiogram
- percutaneous transhepatic biliary drainage
- MRI/MRCP
- early repair
- delayed repair
- hepato-jejunostomy
- repair patency
1. Introduction
Laparoscopic cholecystectomy (LC) continues to be one of the most frequent surgical procedures performed in the US and the world, while bile duct injury (BDI) is the most morbid complication of LC [1]. Multiple preventive techniques reduced this complication rate [2], but BDI is still described in all LC’s at 0.1–0.5% range [3]. Due to the high numbers of cholecystectomies performed, it is an enormous healthcare problem often leading to long-term physical and psychological morbidity to patients, with mortality described up to 7% [4]. It also is associated with multiple interventions and hospitalizations that generate a significant cost and burden to the patient and healthcare system [5].
Prevention of BDI is of paramount importance. Over the years, various classifications of biliary injuries have been proposed, and different methods have been described to prevent iatrogenic biliary tract lesions. The optimal treatment is influenced by the timing of recognition of the injury, the extent of BDI, the patient’s clinical condition, and the availability of experienced hepatobiliary surgeons. This chapter aims to discuss the current updated management of iatrogenic BDI.
2. Safe cholecystectomy and prevention of BDI
2.1 Risk factors
Anatomical:
Different variants of the cystic duct, such as short cystic duct, cystic duct running parallel to the common bile duct (CBD)
Hepato-cystic duct
Accessory cystic duct
Aberrant bile ducts.
Patient-related:
Acute or chronic inflammation
Previous gastrointestinal or biliary surgery
Obesity.
It has been demonstrated that the primary cause of BDI is the misinterpretation of biliary anatomy in 71–97% of all cases [6].
Over the years, various methods have been proposed and described to prevent iatrogenic biliary injury [7, 8, 9].
2.2 Surgical technique
2.2.1 Anatomical landmarks
“Rouvière’s sulcus”-2–5 cm sulcus running to the right of liver hilum, anterior to the caudate lobe, containing the right portal triad or right posterior branches, and usually easily visible during the laparoscopy. It can be considered a useful landmark site to start dissection of the hepato-cystic triangle during LC, and “no-pass” point to prevent the injury of the right hepatic artery [10].
“Cystic lymph node” or Mascagni’s node—always lies lateral to the biliary tree and should form the medial end point of dissection [11].
“B-SAFE method”—by using five anatomic landmarks (B, bile duct; S, Rouvière’s sulcis; A, hepatic artery; F, umbilical fissure; E, enteric/duodenum) to guide the dissection [12].
The “line of safety” (Figure 1)—an imaginary line which extends from Rouviere’s sulcus to the junction of the cystic and hilar plates, near the base of segment 4. It has been recently accepted as a relatively simple to define landmark representing the lower boundary for safe dissection [13].
2.2.2 Dissection approach
Infundibular method—dissection close to gallbladder infundibulum, still carries a risk of identifying dilated cystic duct as an infundibulum, while identifying CBD as a cystic duct [2]
Fundus first/dome-down technique—a way of dissection from the gallbladder fundus up to the infundibulum away from Calot’s triangle, so the gallbladder is left hanging on the cystic artery and cystic duct [14].
2.2.3 Final anatomical identification
The “critical view of safety (CVS)” technique (Figure 2) was introduced by Strasberg in 1995, and it is considered the gold standard to perform a safe cholecystectomy [9, 15]. It implies the identification of biliary structures during dissection and includes 3 criteria:
The hepato-cystic triangle must be cleared of adipose and fibrotic tissues, and the CBD must not be exposed.
The lower third of the gallbladder must be separated from the liver bed to expose the cystic plate.
Two and only two structures should be seen entering the gallbladder.
2.3 Intra-operative tools
2.3.1 Intra-operative cholangiography (IOC)
It has been proposed for the better declaration of biliary anatomy, detection of silent CBD stones, and reduction of incidence of BDIs [16]. The opinions about the “routine” or “selective” use of IOC still represent a matter of debate, but the selective approach is considered to have comparable chances of preventing and detecting BDI [17, 18]. However, it is highly advised to use IOC in any case of difficult LC or when there is a concern about biliary anatomy identification [18, 19].
2.3.2 Intra-operative ultrasound (IOUS)
It was shown to provide a highly sensitive mapping of the extra-hepatic biliary anatomy [20], but the difficult learning curve and the lack of randomized controlled trials have reduced its use in clinical practice.
2.3.3 Fluorescent cholangiography
It represents a novel intra-operative imaging technique that allows real-time enhanced visualization of the extrahepatic biliary tree by fluorescence, after the intravenous injection of the dye indocyanine green (ICG) [21]. It is a safe and useful method that became a common practice in difficult cholecystectomy [22, 23]. However, under the conditions of severe inflammation, this imaging can be less clear, and then, a strong consideration to bail out is suggested (Figure 3).
2.4 When to bail out
“Inflection point”—the moment the decision is made to complete formal laparoscopic cholecystectomy [24].
The general rule is that it should happen sooner than later before the injury happens. The consequences of bailing out are usually less morbid than those of biliary injury.
The following factors may influence personal surgeon’s decision toward the inflection point [24, 25]:
Personal experience
Inability to establish biliary anatomy
Lack of intra-operative imaging modalities
Time since the incision—60 minutes in general or 1.5 times the personal median time for LC completion
Lack of colleague second opinion.
2.5 How to bail out
2.5.1 Laparoscopic subtotal or partial cholecystectomy
2.5.1.1 Fenestration type - preferred method
Fenestration of the gallbladder anterior wall, leaving the posterior wall attached to the liver, ablating the mucosa, and securing the cystic duct at its origin from the mucosal side within the gallbladder [26].
Pros: usually easy recognition of the cystic duct origin, reduced blood loss with no need to dissect the gallbladder bed from the liver, usually no need for a conversion to open procedure.
2.5.1.2 Reconstitution type - optional method: resection of most of the gallbladder and leaving the small stump
Pros: can prevent BDI in complex cases.
Cons: risk for neo-gallbladder appearance, recurrent stones, possible need for cholecystectomy completion, which is likely more complex and high-risk compared to the index one.
2.5.2 Conversion to the open procedure
Pros: usually allows cholecystectomy completion, improved recognition of the anatomy including vascular structures [24, 25, 26].
Cons: morbidity related to the open incision, lack of experience of modern surgeons in open cholecystectomy.
A general recommendation is that in all cases of complicated cholecystectomies, the surgeon must not hesitate when considering bailing out from the completion of formal LC, because the consequences may be dramatic.
3. Diagnosis
3.1 Clinical presentation
Depending on the timing of diagnosis and type of injury, it can be divided as followings by pathophysiology:
3.1.1 Asymptomatic/at the time of LC
3.1.1.1 Biliary leak
The evolution of the symptoms is a function of bile accumulation based on the severity of the leak and is very subtle.
Symptoms are usually non-specific (nausea, vomiting, bloating, widespread abdominal pain, general discomfort, and anorexia) till the development of bile peritonitis and sepsis.
3.1.1.2 Biliary obstruction and stricture
It may have a different natural course based on the degree of obstruction (complete/partial) and location of the lesion (proximal/distal bile duct, main/lobar bile duct).
Symptoms include obstructive jaundice and/or cholangitis, with abdominal pain, jaundice, and signs of infection/sepsis.
3.2 Non-invasive imaging
Radiologic investigations should be obtained for the correct identification of the damage, its extension, and gravity and to plan therapeutic strategies.
3.2.1 Ultrasonography (US)
A primary and easily available diagnostic tool that allows finding fluid collections, dilation of the bile ducts, and possibly associated vascular lesions, using Doppler evaluation [27].
3.2.2 Computed tomography (CT)
Superior to the US in detecting fluid collections, and guiding their percutaneous drainage, but similar to the US is not reliable in distinguishing bile leaks from other postoperative fluid collections, such as blood, pus, or serous fluid, because of their similar densities [28, 29, 30]. It can also show biliary obstruction with upstream dilatation, or long-term sequelae of a long-standing bile stricture, such as lobar hepatic atrophy or signs of secondary biliary cirrhosis. The CT scan is specifically useful to identify any associated vascular lesions.
3.2.3 Hepatobiliary scintigraphy (HS)
It seems to be more sensitive and specific than US or CT in detecting bile leaks and can provide functional information demonstrating the presence of an active leak [31]. However, its spatial resolution is poor, and the identification of the leak site can be challenging. In addition, it is limited in providing the exact anatomy of the whole biliary tree and in patients with hepatic dysfunction, and large leaks have poor sensitivity and can show no extrahepatic bile duct [32]. Because of those limitations, it is rarely used as a standalone test, and its use is replaced mostly by magnetic resonance imaging.
3.2.4 Magnetic resonance imaging with cholangiopancreatography (MRI/MRCP)
A non-invasive “gold standard” for the complete morphological evaluation of the biliary tree as it offers detailed information about the integrity of the biliary tract [28, 33]. The use of a gadolinium contrast agent during MRI/MRCP allows the detection of active bile leakage by direct visualization of contrast material extravasation into fluid collections in addition to demonstrating the anatomical site of the leakage and the type of BDI, and thus, it is superior to CT and US in specifying the collection as biloma [34, 35].
3.3 Invasive cholangiography
3.3.1 Types used
Endoscopic retrograde cholangiopancreatography (ERCP) [32]
Percutaneous transhepatic cholangiography (PTC)
Intra-operative cholangiography (IOC).
3.3.2 General advantages
A “gold standard” in identifying the presence of BDI and its type
Provide exact biliary anatomy
Allows the treatment of the injury by stenting and/or biliary drainage.
3.3.3 General disadvantages
Nonnegligible risk of complications
Lack of detection of extra biliary abnormality and surgical complications
Non-visualization of the biliary tree upstream or downstream of the lesion—in case of complete transection or obstruction of the bile duct may require both ERCP and PTC to complete the biliary anatomy.
3.3.4 Specific considerations
3.3.4.1 ERCP
Treatment of bile leak by papillotomy and pressure reduction and stenting [32, 36]
In advanced injury as bridging till definitive repair in advanced
In low-grade injury, usually with biliary opening less than 5 mm, as a definite treatment with no need for surgical repair
Treatment of biliary obstruction by stenting
Complications: pancreatitis, bleeding, and cholangitis.
3.3.4.2 PTC
Usually requires dilation of the biliary tree, so easier to apply when some degree of biliary obstruction is present [37, 38]
Treatment of bile leak by diversion of the bile flow
When ERCP is not possible or not successful
In the complete transection of the bile duct
Treatment of biliary obstruction by diversion of the bile flow and stenting
Recent experience showed satisfactory results with performing an extraluminal percutaneous endoscopic rendezvous procedure with stent placement to restore continuity of the bile duct [38, 39]. This procedure should be considered with caution, as it carries a risk for significant complications such as choledochoduodenal fistula [40].
Complications: bleeding and cholangitis.
4. Classification
The location of BDI on the biliary tree is of primary importance in deciding management and predicting outcomes. We suggest using classification introduced by Strasberg in 1995 [7], as its comprehensive anatomical and functional injury description allows repair guidance and stratifies the risk for long-term complications, such as biliary stricture [41].
Figure 4 Strasberg classification.
Type A: bile leakage from either the minor bile ducts from gallbladder bed or the cystic duct.
Type B and C: occlusion (type B) or transection (type C) of aberrant right hepatic ducts.
Type D: lateral damage to the common bile duct resulting in a biliary leak.
Type E: involve the main ducts and are classified according to the level of injury in the biliary tree. Each type corresponds to the same type of Bismuth classification:
E1 - >2 cm from the confluence.
E2 - <2 cm from the confluence.
E3 - in the hilum, right and left duct are not separated.
E4 - in the hilum, right and left duct are separated.
E5 - in the hilum, combined with type C.
5. Timing of diagnosis and repair
Early and delayed repair are both acceptable approaches to a definite repair of BDI. The big question exists regarding an exact definition of “early” vs. “delayed”. The data is mixed, and the time from the initial surgery is defined as between 0 and 21 days for early [5, 8, 12, 13] and after 4–6 weeks as “delayed” [8, 12].
Advantages of early approach:
Reduced inflammation—if done early enough
Decreased morbidity of temporary biliary drainage
Decreased psychological trauma to the patient
Faster recovery and a quicker return to the regular lifestyle.
Advantages of delayed approach:
More detailed diagnosis of the degree and type of BDI
Reduction in inflammation
Improved anatomic visualization
Delay allows undiagnosed associated vascular injuries to be identified.
Provides the surgeon a better roadmap for developing an operative plan for definitive reconstruction.
5.1 Choice of the early versus delayed repair
5.1.1 Timing
Based on most recent evidence, we recommend considering early repair within 48–72 hours from the injury [40, 42, 43]. Some data suggests the earlier the repair, the better the results [4, 44, 45] whereas other support comparable good outcomes within 72 hours timeframe [46].
When missed the opportunity window of 48–72 hours for an early repair, it is advised to delay it for at least 4–6 weeks [37, 43, 47]. This will allow to decrease the degree of local inflammation, control infection, and optimize the conditions for a complex reconstruction.
5.1.2 Expertise
The repair of a bile duct injury is a complicated procedure, and there is clear evidence that the best results are obtained at a center with experienced hepatobiliary surgeons [43, 48, 49, 50]. It is a single most important factor in the success of the repair. At attempt to perform an immediate repair by an unexperienced surgeon is associated with worse outcomes and can compromise the future repair by a specialist, in case of repair complications [43, 50].
5.2 Early repair
5.2.1 Immediate recognition of the injury at the time of LC
After the prevention of the injury, the surgeon’s awareness to suspect and evaluate for a BDI is the second most important factor in determining the patient prognosis.
5.2.1.1 Immediate intra-operative repair
If the required surgical expertise is present, we suggest following steps:
Conversion to an open procedure
Careful surgical exploration and identification of important structures and the injury
Confirmation of injury type with intra-operative cholangiography
The preference is to image both proximal and distal direction of the biliary tree if possible.
Consider IOUS if vascular injury is suspected [51]
Immediate repair according to the type of injury.
5.2.1.2 Early transfer to a tertiary referral center
If the competent surgeon capable of performing a biliary reconstruction is not present, we advise to follow the next steps:
DO NOT convert to an open procedure. This may expose the patient to an additional morbidity and make the definite repair more complicated [43, 48, 50]. The acceptable reason to convert may be bleeding difficult to control laparoscopically.
If possible, evaluate the injury type by intra-operative cholangiogram.
Place a drain [52].
Transfer a patient as soon as possible to a tertiary hepatobiliary referral center—that provides better outcomes that immediate repair by less experienced surgeon.
Provide as much relevant information as possible with the referral. Additional imaging, such as MRI/MRCP, can be performed while waiting for a transfer.
5.2.2 Early recognition after completion of cholecystectomy
At the same admission it presents as described earlier symptoms and signs of biliary leak, obstruction, or both. A general recommendation is that any alteration in the normal postoperative course after LC must suggest a possible damage to the biliary tract. Sometimes, the evolution of biliary symptoms is subtle, so high degree of clinical suspicion and careful clinical evaluation of patients are essential. It will allow the thorough and prompt inpatient evaluation and/or referral to a tertiary specialty center.
The diagnosis after the discharge is often made based on clinical symptoms, which means more advanced and complicated problem, or based on abnormal lab tests, in case of milder injury.
To allow the chance of early repair, one should apply similar principles as described in case of intra-operative injury recognition:
5.2.2.1 Perform prompt biliary imaging to evaluate the type of the injury and provide the drainage of biliary system
US:
Initial imaging
Identification of biliary dilatation, fluid collections, and vascular injuries by Doppler.
MRCP:
First-line non-invasive imaging.
Can be confirmatory for the type of injury.
CT:
Important to rule out associated vascular injury
Allows imaging-guided percutaneous drainage of the collections.
ERCP:
First-line confirmatory biliary imaging.
Allows drainage and stenting.
In mild grade injuries (A-D) can be sufficient as the only treatment with no need for operative intervention.
PTC:
First-line procedure for drainage and stenting when MRI/MRCP confirms complete transection or obstruction of the bile ducts
Usually needed in type E injuries is temporary bridging treatment till the delayed repair [40]
Second-line procedure for drainage and stenting if ERCP not feasible.
Drain any biloma or abscess percutaneously if operative drain is not present or is not providing adequate drainage—to prevent and treat bile peritonitis and sepsis, as well as to control the ongoing leak [52].
5.2.2.2 Make the decision about the possibility of early repair, based on factors discussed earlier
Presence of competent hepatobiliary surgeon
Timing of the diagnosis—up to 72 hours from the injury
Absence of vascular injury.
5.3 Delayed repair
5.3.1 The conditions leading to choosing the delayed repair approach
Late recognition—beyond 72 hours from the injury
Need for a comprehensive work-up to determine the type and degree of the injury
Delays in transfer to a referral hepatobiliary center, related to geographic distance, transportation resources, and bed availability [40, 53]
Patient hemodynamic instability or uncontrolled sepsis [52]
Patient complex medical background requiring pre-operative optimization [40].
6. Management and repair of minor BDI—types A-D
6.1 Type A injury
6.1.1 Non-operative management
6.1.2 Operative repair
The operative intervention reserved for minority of the cases, where the leak is not resolving after ERCP and drainage or when discovered intra-operatively
Technique—surgical ligation of a cystic duct stump or oversewing an accessory duct at the gallbladder bed provides simple and reliable solution.
6.2 Type B injury
6.2.1 Non-operative management
Is appropriate when a segmental or accessory ligated duct is small (usually up to 3 mm) and cholangiography demonstrates adequate drainage of the segment with an injured bile duct.
Temporary percutaneous drainage (PTC) can be placed to control cholangitis in the obstructed segment.
6.2.2 Operative repair
Is warranted if the injured duct is bigger (more than 3 mm), drain multiple hepatic segments, no adequate drainage is confirmed by cholangiography or if there is recurrent cholangitis is present despite maximal percutaneous drainage
Reconstruction of injured duct by Roux n Y Hepato-Jejunostomy—when duct is bigger, and reconstruction is technically feasible
Hepatic resection of the obstructed segment to control recurrent cholangitis—when reconstruction is not feasible.
6.3 Type C injury
6.3.1 Non-operative management
Is appropriate when segmental or accessory leaking duct is small (up to 2–3 mm), cholangiography demonstrates adequate drainage of the segment with an injured bile duct.
Temporary endoscopic or percutaneous drainage may be required to control the leak.
6.3.2 Operative repair
Ligation of injured duct—when the duct is small and adequate segmental drainage confirmed by cholangiography, but the leak is not controlled.
Reconstruction of injured duct by Roux n Y Hepato-Jejunostomy—when the duct is large, and no adequate drainage is confirmed by cholangiography.
Injuries grade D and above usually will require operative intervention.
6.4 Type D injury
6.4.1 Non-operative management
ERCP with papillotomy and possible stenting can be appropriate when the side injury of the bile duct is small, usually less than 5 mm, and the leak is low output [49, 56].
Can be attempted on the high-output leaks as well, but the chance for success with endoscopic treatment only is low [54]
In addition, an abdominal drain for controlling the leak should be placed [49, 54].
6.4.2 Operative repair
Is recommended if recognized intra-operatively, after the failure of endoscopic treatment or large injury and leak are demonstrated on the imaging [49, 56, 57, 58]
Usually, the choledochotomy can be repaired primarily with 5–0 or 6–0 absorbable sutures.
In case of very large side injury, debridement of the duct may be required and primary duct-to-duct anastomosis with healthy duct edges performed [45, 60].
Consider surgical or endoscopic stenting in addition to the surgical repair [45, 61, 62].
7. Management and repair of major BDI—types E injury (transection, clipping, or stricture of major bile ducts)
7.1 Non-operative management
7.1.1 ERCP
Rarely can be successful as a standalone management without surgical reconstruction and is associated with high morbidity [54, 63]
Consider as an alternative for surgical reconstruction in patients with very-high perioperative risk due to medical co-morbidities and surgical history [40]
Can be attempted when there is at least partially documented MRCP confirmed of the bile duct, or a very close proximity of the proximal and distal biliary stumps two biliary stumps [64]
This should be performed only by highly experienced biliary endoscopist, as it might carry the risk for significant morbidity endoscopists [40, 60, 63, 64].
Although less investigated in the literature, long-term (at 10 years) outcomes of endoscopic treatment with stent placement appeared to be good and effective in patients with postoperative biliary strictures [65, 66, 67].
7.1.2 PTC
A necessary and effective bridging biliary procedure while waiting for a delayed repair [40, 67, 68]
Specifically successful in cases of complete obstruction of the bile duct, or when a significant stricture present, and ERCP is not successful or feasible [67, 68]
PTC in the presence of bile leakage may be more difficult because of non-dilated bile ducts but still leads to a technical success of 90% and a short-term clinical success of 70–80% in expertise centers [67, 68, 69].
7.2 Primary anastomosis of the bile duct-choledocholedochostomy
7.2.1 Why to attempt-advantages on bilioenteric reconstruction
Less technically complex
Shorter operative time-important in case the patient is septic or unstable.
Less short-term post-operative complications [70].
Allows favorable access for endoscopic treatment of anastomotic complications.
7.2.2 Can be performed in selected cases-conditions to perform
If there is no significant loss of bile duct tissue (usually less than 1 cm)
Proximal and distal biliary stump ends can be opposed without tension.
Recommended in settings of early reconstruction only, usually not feasible in a delayed fashion, as the chronic inflammation and fibrosis interferes with an ability to perform tension free repair [57, 71]
When no vascular injury is present
7.2.3 An exceptional clinical judgment is required to decide about the primary bile duct
reconstruction as this approach is associated with increased failure rate compared to bilioenteric reconstruction, especially when it is performed beyond the conditions mentioned above [50, 57, 72].
7.2.4 Choledocholedochostomy-operative technique
Debridement of bile duct ends, till getting satisfactory healthy tissue
Extended Kocher maneuver can help with mobilization of a distal bile duct and allow approximation of both ends
Consider placement of biliary stent or T-tube
Performing an end-to-end fashion anastomosis with absorbable sutures.
Drain placement.
7.3 Bilioenteric reconstruction—Roux-en-Y hepatojejunostomy
It represents a gold standard surgical repair of major bile duct injuries and is being performed as a definite repair in most cases of BDI [7, 43, 49, 73]
7.3.1 Advantages
Allows resection of the bile duct and performing high biliary anastomosis
It which carries better blood supply by communicating vessels from peribiliary plexus at the level of biliary bifurcation, which usually remain intact even after high grade BDI
Allows tension-free anastomosis
Overall, less anastomotic complication and reduced need for reoperation than the primary bile duct repair [50, 57, 72, 73, 74].
7.3.2 Roux-en-Y Hepato-jejunostomy-surgical technique
Closure of the distal bile duct stump
Proximal small bowel Roux limb creation
Placement of biliary stent through the anastomosis
End-to-side or side-to-side proximal bile duct-to-bowel anastomosis with absorbable sutures
Creation of Y limb and jejunojejunostomy (Figure 5).
7.3.3 The details of repair vary depending upon the grade of the injury
7.3.3.1 Type E1–2
Single duct bilioenteric anastomosis.
7.3.3.2 Type E3
If the bile duct bifurcation maintained as a single orifice allowing technically feasible reconstruction—can perform single bilioenteric anastomosis
If not, two separate right and left anastomoses should be performed.
7.3.3.3 Type E4
Two separate right and left biliary enteric anastomoses are usually required.
As an alternative both biliary branches can be reconstructed together as a single orifice.
In rare cases, suitable duct length outside the hepatic parenchyma cannot be obtained, these cases necessitate isolation of the intrahepatic biliary system, and IOUS may be necessary in these situations.
7.3.3.4 Type E5
Principles of E4 type are applied.
The additional duct may be ligated or reconstructed based on the principles for segmental accessory duct injury management, described earlier.
7.3.3.5 Technical solutions in complicated cases
8. Vasculobiliary injury (VBI)
This is defined as a combined injury to a bile duct and to an accompanying major blood vessels in the porta hepatis.
Types of VBI [75]:
Classic (over 90% of VBI)—Right hepatic artery (RHA) injury
Extreme (less than 10% of VBI)—Combined RHA and main or right portal vein (PV) injury.
8.1 Classic VBI
8.1.1 Injury to the RHA below the biliary confluence (usually type E1/E2)
Does not usually cause a clinically significant ischemic injury to the liver parenchyma, due to a shunt that occurs immediately from the left hepatic artery (LHA) traveling via the transverse hilar marginal artery (THMA) to the right liver [76].
8.1.2 Injury to the RHA above the biliary confluence of the ducts
Will disrupt the collateral biliary blood supply including THMA.
Possible clinical presentations include development of small areas of right hepatic lobe ischemia with possible subsequent abscesses formation.
Chronic atrophy of the right hepatic lobe, which is usually clinically unsignificant due to intact portal blood supply.
8.2 Impact of VBI on definite repair approach
8.2.1 Diagnosis
US with Doppler can provide some information.
CT scan with IV contrast usually required as a part of work-up for high-grade biliary injury (types E) to rule out.
High level of suspicion for VBI, based on high grade biliary injury or intra-operative bleeding will mandate the imaging work-up, making the immediate repair unlikely.
8.2.2 Timing of repair
VBI increases the risk for repair stenosis repair should not be neglected as it will lead to extensive morbidity and the need for endoscopic or percutaneous interventions [75].
In severe and untreated cases, it can lead to late biliary cirrhosis with portal hypertension.
To avoid this the repair should be delayed for several weeks to allow the ischemic injury to delineate and ensure the anastomosis is done to well vascularized tissue.
8.2.3 Surgical approach to repair
Hepaticojejunostomy is the repair of choice.
A resection of extrahepatic bile duct and the anastomosis at the level of bifurcation is preferred—to achieve adequately perfused margins.
While lowering the hilar plate to achieve sufficient proximal biliary stump, care should be taken to avoid additional devascularization of peribiliary vascular plexus.
Described above side-to-side hepato-jejunostomy technique can provide a solution for creation of wide and well-vascularized anastomosis.
8.2.4 Arterial reconstruction
Usually, it is not possible to reconstruct the RHA and indeed it is not necessary, because of little clinical significance of liver disfunction.
8.2.5 Outcomes
With the right surgical classic VBI can be managed with the outcomes comparable to BDI without vascular injury [40].
8.3 Extreme VBI
Rare and devastating injury
Can be associated with “dome-down” approach to a shrunken gallbladder which results in massive bleeding from both the portal vein and hepatic artery [77].
The main priority—bleeding control
As opposed to arterial injury, the likelihood of hepatic ischemia is high in PV injury.
It can require right hepatectomy in case of RPV injury or PV reconstruction and even liver transplantation in case of main PV injury.
In this scenario, the short- and long-term outcomes are dismal with up to 60% mortality risk [78].
9. Conclusions
Bile duct injury (BDI) remains a critical complication following cholecystectomy.
Early recognition and appropriate management can significantly improve patient outcomes.
Prevention of biliary injury during cholecystectomy is of paramount importance and includes recognition of anatomical landmarks and a critical view of safety achievement, precise surgical technique, use of intra-operative imaging, and timely bailing out from a completion of a standard laparoscopic cholecystectomy.
Diagnosis of biliary injury is made based on clinical picture of biliary leak or obstruction, ultrasonography, cross-sectional imaging, and cholangiography.
Strasberg classification of BDI is the most comprehensive to define the type and extent of the injury and guide the surgical repair.
Early and delayed repair are both acceptable approaches to a definite repair of BDI. We recommend choosing an early repair up to 72 hours from the injury and if missed this opportunity, to delay it for at least 4 weeks.
The BDI repair should be performed by an experienced Hepato-Pancreato-Biliary surgeon, and thus, the presence of such an expertise is the most important factor in deciding the timing of the repair.
If needed, early and organized referral to a tertiary center is the first time limiting critical step of BDI management.
Intraoperative recognition of the injury allows the best chance for an early repair and can prevent the morbidity associated with a delayed repair.
Prior to a decision for the repair, the complete understanding of biliary anatomy and injury type is required and can be achieved by MRI/MRCP, ERCP or PTC.
The latter two are also important for a temporary control of biliary injury.
PTC is particularly useful as a bridging treatment for high-grade injuries with a loss of biliary continuity while waiting for a delayed repair.
As a part of surgical management, the intra-abdominal biliary sepsis and leak should be controlled with appropriate drainage.
The definite surgical management of low-grade Strasberg types A-D injuries can include biliary drainage only, primary repair of the bile duct or duct-to-duct biliary reconstruction.
In cases of significant bile duct tissue loss and tension associated with primary repair, bilioenteric reconstruction with Roux-en-Y hepato-jejunostomy is recommended.
High-grade Strasberg type E injuries should be always repaired with Roux-en-Y hepatojejunostomy.
The proper surgical technique allowing reconstruction of healthy and well-vascularized bile duct is an absolute condition for a success and long-term patency of the repair, so the resection of the extrahepatic bile duct and high anastomosis at the level of biliary bifurcation is always preferred.
Associate vascular injury defined as vasculobiliary injury (VBI) should be always ruled out in BDI evaluation.
Most common is right hepatic artery injury and it mandates delaying the definite surgical repair to allow the ischemic injury to delineate and ensure the anastomosis is done to well-vascularized tissue.
With appropriate management, comparable outcomes to BDI without vascular injury can be achieved.
Rare and devastating portal vein injuries often require partial liver resections and are associated with high morbidity and mortality.
Acknowledgments
Chirag S Desai, MD, University of North Carolina at Chapel Hill, Division of Abdominal Transplantation for the mentorship, guidance, and friendship.
Thanks
Thanks to my family, colleagues, and mentors, this book chapter publishing would not be possible without their support.
References
- 1.
Ingraham AM, Cohen ME, Ko CY, Hall BL. A current profile and assessment of north American cholecystectomy: Results from the American college of surgeons national surgical quality improvement program. Journal of the American College of Surgeons. 2010; 211 :176-186 - 2.
Daly SC, Deziel DJ, Li X, et al. Current practices in biliary surgery: Do we practice what we teach? Surgical Endoscopy. 2016; 30 :3345-3350 - 3.
Stilling NM, Fristrup C, Wettergren A, et al. Long-term outcome after early repair of iatrogenic bile duct injury. A national Danish multicentre study. HPB. 2015; 17 :394-400 - 4.
Pekolj J, Alvarez FA, Palavecino M, Sa’nchez Claria R, Mazza O, de Santibañes E. Intraoperative management and repair of bile duct injuries sustained during 10,123 laparoscopic cholecystectomies in a high-volume Re- ferral Center. Journal of the American College of Surgeons. 2013; 216 :894-901 - 5.
Booij KAC, de Reuver PR, van Dieren S, et al. Long-term impact of bile duct injury on morbidity, mortality, quality of life, and work related limitations. Annals of Surgery. Jul 2018; 268 (1):143-150 - 6.
Nuzzo G, Giuliante F, Giovannini I, Ardito F, D'Acapito F, Vellone M, et al. Bile duct injury during laparoscopic cholecystectomy: Results of an Italian national survey on 56 591 cholecystectomies. Archives of Surgery. 2005; 140 (10):986-992. DOI: 10.1001/archsurg.140.10.986 - 7.
Strasberg SM, Hertl M, Soper NJ. An analysis of the problem of biliary injury during laparoscopic cholecystectomy. Journal of the American College of Surgeons. 1995; 180 (1):101-125 - 8.
Pesce A, Palmucci S, La Greca G, Puleo S. Iatrogenic bile duct injury: Impact and management challenges. Clinical and Experimental Gastroenterology. 2019; 12 :121-128. DOI: 10.2147/CEG.S169492 - 9.
Strasberg Steven M, Michael BL. The critical view of safety: Why it is not the only method of ductal identification within the standard of care in laparoscopic cholecystectomy. Annals of Surgery. 2017; 265 (3):464-465. DOI: 10.1097/SLA.0000000000002054 - 10.
Hugh TB, Kelly MD, Mekisic A. Rouvière's sulcus: A useful landmark in laparoscopic cholecystectomy. The British Journal of Surgery. 1997; 84 (9):1253-1254. DOI: 10.1046/j.1365-2168.1997.02769.x - 11.
Ferzli G, Timoney M, Nazir S, Swedler D, Fingerhut A. Importance of the node of calot in gallbladder neck dissection: An important landmark in the standardized approach to the laparoscopic cholecystectomy. Journal of Laparoendoscopic & Advanced Surgical Techniques. Part A. 2015; 25 (1):28-32. DOI: 10.1089/lap.2014.0195 - 12.
Sutherland F, Dixon E. The importance of cognitive map placement in bile duct injuries. Canadian Journal of Surgery. 2017; 60 (6):424-425. DOI: 10.1503/cjs.008816 - 13.
Greene B, Tsang M, Jayaraman S. The inferior boundary of dissection as a novel landmark for safe laparoscopic cholecystectomy. HPB: The Official Journal of the International Hepato Pancreato Biliary Association. 2021; 23 (7):981-983. DOI: 10.1016/j.hpb.2021.02.004 - 14.
Neri V, Ambrosi A, Fersini A, Tartaglia N, Valentino TP. Antegrade dissection in laparoscopic cholecystectomy. Journal of the Society of Laparoscopic Surgeons. 2007; 11 (2):225-228 - 15.
Strasberg SM, Brunt LM. Rationale and use of the critical view of safety in laparoscopic cholecystectomy. Journal of the American College of Surgeons. 2010; 211 (1):132-138. DOI: 10.1016/j.jamcollsurg.2010.02.053 - 16.
Pesce A, Portale TR, Minutolo V, Scilletta R, Li Destri G, Puleo S. Bile duct injury during laparoscopic cholecystectomy without intraoperative cholangiography: A retrospective study on 1100 selected patients. Digestive Surgery. 2012; 29 (4):310-314. DOI: 10.1159/000341660 - 17.
Sajid MS, Leaver C, Haider Z, Worthington T, Karanjia N, Singh KK. Routine on-table cholangiography during cholecystectomy: A systematic review. Annals of the Royal College of Surgeons of England. 2012; 94 (6):375-380. DOI: 10.1308/003588412X13373405385331 - 18.
Törnqvist B, Strömberg C, Akre O, Enochsson L, Nilsson M. Selective intraoperative cholangiography and risk of bile duct injury during cholecystectomy. The British Journal of Surgery. 2015; 102 (8):952-958. DOI: 10.1002/bjs.9832 - 19.
Törnqvist B, Waage A, Zheng Z, Ye W, Nilsson M. Severity of acute cholecystitis and risk of iatrogenic bile duct injury during cholecystectomy, a population-based case-control study. World Journal of Surgery. 2016; 40 (5):1060-1067. DOI: 10.1007/s00268-015-3365-1 - 20.
Dili A, Bertrand C. Laparoscopic ultrasonography as an alternative to intraoperative cholangiography during laparoscopic cholecystectomy. World Journal of Gastroenterology. 2017; 23 (29):5438-5450. DOI: 10.3748/wjg.v23.i29.5438 - 21.
Ishizawa T, Bandai Y, Kokudo N. Fluorescent cholangiography using indocyanine green for laparoscopic cholecystectomy: An initial experience. Archives of Surgery. 2009; 144 (4):381-382. DOI: 10.1001/archsurg.2009.9 - 22.
Pesce A, Piccolo G, La Greca G, Puleo S. Utility of fluorescent cholangiography during laparoscopic cholecystectomy: A systematic review. World Journal of Gastroenterology. 2015; 21 (25):7877-7883. DOI: 10.3748/wjg.v21.i25.7877 - 23.
Calabro KA, Harmon CM, Vali K. Fluorescent cholangiography in laparoscopic cholecystectomy and the use in Pediatric patients. Journal of Laparoendoscopic & Advanced Surgical Techniques. Part A. 2020; 30 (5):586-589. DOI: 10.1089/lap.2019.0204 - 24.
Strasberg SM. A three-step conceptual roadmap for avoiding bile duct injury in laparoscopic cholecystectomy: An invited perspective review. Journal of Hepato-Biliary-Pancreatic Sciences. 2019; 26 (4):123-127. DOI: 10.1002/jhbp.616 - 25.
Bourgouin S, Mancini J, Monchal T, Calvary R, Bordes J, Balandraud P. How to predict difficult laparoscopic cholecystectomy? Proposal for a simple preoperative scoring system. American Journal of Surgery. 2016; 212 (5):873-881. DOI: 10.1016/j.amjsurg.2016.04.003 - 26.
Bornman PC, Terblanche J. Subtotal cholecystectomy: For the difficult gallbladder in portal hypertension and cholecystitis. Surgery. 1985; 98 (1):1-6 - 27.
Wigham A, Alexander GL. Radiologic assessment of hepatobiliary surgical complications. Seminars in Ultrasound, CT, and MR. 2013; 34 (1):18-31. DOI: 10.1053/j.sult.2012.11.002 - 28.
Jabłońska B, Lampe P. Iatrogenic bile duct injuries: Etiology, diagnosis and management. World Journal of Gastroenterology. 2009; 15 (33):4097-4104. DOI: 10.3748/wjg.15.4097 - 29.
Mulé S, Colosio A, Cazejust J, Kianmanesh R, Soyer P, Hoeffel C. Imaging of the postoperative liver: Review of normal appearances and common complications. Abdominal Imaging. 2015; 40 (7):2761-2776. DOI: 10.1007/s00261-015-0459-z - 30.
Lee CM, Stewart L, Way LW. Postcholecystectomy abdominal bile collections. Archives of Surgery. 2000; 135 (5):538-542. DOI: 10.1001/archsurg.135.5.538 - 31.
Tripathi M, Chandrashekar N, Kumar R, Thomas EJ, Agarwal S, Bal CS, et al. Hepatobiliary scintigraphy. An effective tool in the management of bile leak following laparoscopic cholecystectomy. Clinical Imaging. 2004; 28 (1):40-43. DOI: 10.1016/S0899-7071(03)00035-4 - 32.
Barkun AN, Rezieg M, Mehta SN, Pavone E, Landry S, Barkun JS, et al. Postcholecystectomy biliary leaks in the laparoscopic era: Risk factors, presentation, and management. McGill Gallstone Treatment Group. Gastrointestinal Endoscopy. 1997; 45 (3):277-282. DOI: 10.1016/s0016-5107(97)70270-0 - 33.
Reddy S, Lopes Vendrami C, Mittal P, Borhani AA, Moreno CC, Miller FH. MRI evaluation of bile duct injuries and other post-cholecystectomy complications. Abdominal Radiology (NY). 2021; 46 (7):3086-3104. DOI: 10.1007/s00261-020-02947-z - 34.
Palmucci S, Mauro LA, La Scola S, Incarbone S, Bonanno G, Milone P, et al. Magnetic resonance cholangiopancreatography and contrast-enhanced magnetic resonance cholangiopancreatography versus endoscopic ultrasonography in the diagnosis of extrahepatic biliary pathology. La Radiologia Medica. 2010; 115 (5):732-746. DOI: 10.1007/s11547-010-0526-z - 35.
Aduna M, Larena JA, Martín D, Martínez-Guereñu B, Aguirre I, Astigarraga E. Bile duct leaks after laparoscopic cholecystectomy: Value of contrast-enhanced MRCP. Abdominal Imaging. 2005; 30 (4):480-487. DOI: 10.1007/s00261-004-0276-2 - 36.
Rainio M, Lindström O, Udd M, Haapamäki C, Nordin A, Kylänpää L. Endoscopic therapy of biliary injury after cholecystectomy. Digestive Diseases and Sciences. 2018; 63 (2):474-480. DOI: 10.1007/s10620-017-4768-7 - 37.
Fidelman N, Kerlan RK Jr, Laberge JM, Gordon RL. Accuracy of percutaneous transhepatic cholangiography in predicting the location and nature of major bile duct injuries. Journal of Vascular and Interventional Radiology. 2011; 22 (6):884-892. DOI: 10.1016/j.jvir.2011.02.007 - 38.
Schreuder AM, Booij KAC, de Reuver PR, van Delden OM, van Lienden KP, Besselink MG, et al. Percutaneous-endoscopic rendezvous procedure for the management of bile duct injuries after cholecystectomy: Short- and long-term outcomes. Endoscopy. 2018; 50 (6):577-587. DOI: 10.1055/s-0043-123935 - 39.
Lindemann J, Kloppers C, Burmeister S, Bernon M, Jonas E. Mind the gap! Extraluminal percutaneous-endoscopic rendezvous with a self-expanding metal stent for restoring continuity in major bile duct injury: A case series. International Journal of Surgery Case Reports. 2019; 60 :340-344. DOI: 10.1016/j.ijscr.2019.06.059 - 40.
Zendel A, Kumar A, Serrano P, de Oliveira GC, Button J, Gebre B, et al. Management of major injuries to the bile duct at a hepatobiliary specialty referral center. The American Surgeon. 16 Feb 2022:31348211063553. DOI: 10.1177/00031348211063553. PMID: 35172613. [Epub ahead of print] - 41.
Walsh RM, Henderson JM, Vogt DP, Brown N. Long-term outcome of biliary reconstruction for bile duct injuries from laparoscopic cholecystectomies. Surgery. 2007; 142 (4):450-456. DOI: 10.1016/j.surg.2007.07.008 - 42.
Stewart L. Iatrogenic biliary injuries: Identification, classification, and management. Surgical Clinics. 2014; 94 (2):297-310 - 43.
Wang X, Yu WL, Fu XH, Zhu B, Zhao T, Zhang YJ. Early versus delayed surgical repair and referral for patients with bile duct injury: A systematic review and meta-analysis. Annals of Surgery. 2020; 271 (3):449-459 - 44.
Rystedt J, Lindell G, Montgomery A. Bile duct injuries associated with 55,134 cholecystectomies: Treatment and outcome from a National Perspective. World Journal of Surgery. 2016; 40 (1):73-80. DOI: 10.1007/s00268-015-3281-4 - 45.
Silva MA, Coldham C, Mayer AD, Bramhall SR, Buckels JA, Mirza DF. Specialist outreach service for on-table repair of iatrogenic bile duct injuries - A new kind of 'travelling surgeon'. Annals of the Royal College of Surgeons of England. 2008; 90 (3):243-246. DOI: 10.1308/003588408X261663 - 46.
Dominguez-Rosado I, Sanford DE, Liu J, Hawkins WG, Mercado MA. Timing of surgical repair after bile duct injury impacts postoperative complications but not Anas - Tomotic patency. Annals of Surgery. 2016; 264 (3):544-553 - 47.
Lillemoe KD, Melton GB, Cameron JL, Pitt HA, Campbell KA, Talamini MA, et al. Postoperative bile duct strictures: Management and outcome in the 1990s. Annals of Surgery. 2000 Sep; 232 (3):430-441. DOI: 10.1097/00000658-200009000-00015 - 48.
Strasberg SM. Biliary injury in laparoscopic surgery: Part 2. Changing the culture of cholecystectomy. Journal of the American College of Surgeons. 2005; 201 (4):604-611. DOI: 10.1016/j.jamcollsurg.2005.04.032 - 49.
Perera MT, Silva MA, Hegab B, Muralidharan V, Bramhall SR, Mayer AD, et al. Specialist early and immediate repair of post-laparoscopic cholecystectomy bile duct injuries is associated with an improved long-term outcome. Annals of Surgery. 2011; 253 (3):553-560. DOI: 10.1097/SLA.0b013e318208fad3 - 50.
Stewart L, Way LW. Bile duct injuries during laparoscopic cholecystectomy. Factors that influence the results of treatment. Archives of Surgery. 1995 Oct; 130 (10):1123-1128. DOI: 10.1001/archsurg.1995.01430100101019 - 51.
Alves A, Farges O, Nicolet J, Watrin T, Sauvanet A, Belghiti J. Incidence and consequence of an hepatic artery injury in patients with postcholecystectomy bile duct strictures. Annals of Surgery. 2003; 238 (1):93-96. DOI: 10.1097/01.sla.0000074983.39297.c5 - 52.
Krige JE, Bornman PC, Kahn D. Bile leaks and sepsis: Drain now, fix later. Archives of Surgery. 2010; 145 (8):763. DOI: 10.1001/archsurg.2010.154 - 53.
Ray S, Sanyal S, Das S, Jana K, Das AK, Khamrui S. Outcomes of surgery for post-cholecystectomy bile duct injuries: An audit from a tertiary referral center. Journal of Visceral Surgery. 2020; 157 (1):3-11. DOI: 10.1016/j.jviscsurg.2019.08.005 - 54.
Kimura T, Suzuki K, Umehara Y, Kawabe A, Wada H. Features and management of bile leaks after laparoscopic cholecystectomy. Journal of Hepato-Biliary-Pancreatic Surgery. 2005; 12 (1):61-64. DOI: 10.1007/s00534-004-0935-2 - 55.
Fatima J, Barton JG, Grotz TE, Geng Z, Harmsen WS, Huebner M, et al. Is there a role for endoscopic therapy as a definitive treatment for post-laparoscopic bile duct injuries? Journal of the American College of Surgeons. 2010; 211 (4):495-502. DOI: 10.1016/j.jamcollsurg.2010.06.013 - 56.
Zerem E, Omerović S. Minimally invasive management of biliary complications after laparoscopic cholecystectomy. European Journal of Internal Medicine. 2009; 20 (7):686-689. DOI: 10.1016/j.ejim.2009.07.010 - 57.
Walsh RM, Vogt DP, Ponsky JL, Brown N, Mascha E, Henderson JM. Management of failed biliary repairs for major bile duct injuries after laparoscopic cholecystectomy. Journal of the American College of Surgeons. 2004; 199 (2):192-197. DOI: 10.1016/j.jamcollsurg.2004.02.029 - 58.
Agarwal N, Sharma BC, Garg S, Kumar R, Sarin SK. Endoscopic management of postoperative bile leaks. Hepatobiliary & Pancreatic Diseases International. 2006; 5 (2):273-277 - 59.
ASGE Standards of Practice Committee, Chathadi KV, Chandrasekhara V, Acosta RD, Decker GA, Early DS, et al. The role of ERCP in benign diseases of the biliary tract. Gastrointestinal Endoscopy. 2015; 81 (4):795-803. DOI: 10.1016/j.gie.2014.11.019 - 60.
de Reuver PR, Rauws EA, Vermeulen M, Dijkgraaf MG, Gouma DJ, Bruno MJ. Endoscopic treatment of post-surgical bile duct injuries: Long term outcome and predictors of success. Gut. 2007; 56 (11):1599-1605. DOI: 10.1136/gut.2007.123596 - 61.
Gazzaniga GM, Filauro M, Mori L. Surgical treatment of iatrogenic lesions of the proximal common bile duct. World Journal of Surgery. 2001; 25 (10):1254-1259. DOI: 10.1007/s00268-001-0105-5 - 62.
Pekolj J, Alvarez FA, Palavecino M, Sánchez Clariá R, Mazza O, de Santibañes E. Intraoperative management and repair of bile duct injuries sustained during 10,123 laparoscopic cholecystectomies in a high-volume referral center. Journal of the American College of Surgeons. 2013; 216 (5):894-901. DOI: 10.1016/j.jamcollsurg.2013.01.051 - 63.
Canena J, Horta D, Coimbra J, Meireles L, Russo P, Marques I, et al. Outcomes of endoscopic management of primary and refractory postcholecystectomy biliary leaks in a multicentre review of 178 patients. BMC Gastroenterology. 2015; 15 :105. DOI: 10.1186/s12876-015-0334-y - 64.
Pioche M, Ponchon T. Management of bile duct leaks. Journal of Visceral Surgery. 2013; 150 (3 Suppl):S33-S38. DOI: 10.1016/j.jviscsurg.2013.05.004 - 65.
Costamagna G, Pandolfi M, Mutignani M, Spada C, Perri V. Long-term results of endoscopic management of postoperative bile duct strictures with increasing numbers of stents. Gastrointestinal Endoscopy. 2001; 54 (2):162-168. DOI: 10.1067/mge.2001.116876 - 66.
Costamagna G, Tringali A, Perri V, Familiari P, Boškoski I, Barbaro F, et al. Endotherapy of postcholecystectomy biliary strictures with multiple plastic stents: Long-term results in a large cohort of patients. Gastrointestinal Endoscopy. 2020; 91 (1):81-89. DOI: 10.1016/j.gie.2019.05.042 - 67.
Schreuder AM, Busch OR, Besselink MG, Ignatavicius P, Gulbinas A, Barauskas G, et al. Long-term impact of iatrogenic bile duct injury. Digestive Surgery. 2020; 37 (1):10-21. DOI: 10.1159/000496432 - 68.
Eum YO, Park JK, Chun J, Lee SH, Ryu JK, Kim YT, et al. Non-surgical treatment of post-surgical bile duct injury: Clinical implications and outcomes. World Journal of Gastroenterology. 2014; 20 (22):6924-6931. DOI: 10.3748/wjg.v20.i22.6924 - 69.
de Jong EA, Moelker A, Leertouwer T, Spronk S, Van Dijk M, van Eijck CH. Percutaneous transhepatic biliary drainage in patients with postsurgical bile leakage and nondilated intrahepatic bile ducts. Digestive Surgery. 2013; 30 (4–6):444-450. DOI: 10.1159/000356711 - 70.
Jabłońska B, Lampe P, Olakowski M, Górka Z, Lekstan A, Gruszka T. Hepaticojejunostomy vs. end-to-end biliary reconstructions in the treatment of iatrogenic bile duct injuries. Journal of Gastrointestinal Surgery. 2009; 13 (6):1084-1093. DOI: 10.1007/s11605-009-0841-7 - 71.
Thomson BN, Parks RW, Madhavan KK, Wigmore SJ, Garden OJ. Early specialist repair of biliary injury. The British Journal of Surgery. 2006; 93 (2):216-220. DOI: 10.1002/bjs.5194 - 72.
Huang Q, Yao HH, Shao F, Wang C, Hu YG, Hu S, et al. Analysis of risk factors for postoperative complication of repair of bile duct injury after laparoscopic cholecystectomy. Digestive Diseases and Sciences. 2014; 59 (12):3085-3091. DOI: 10.1007/s10620-014-3255-7 - 73.
Maddah G, Rajabi Mashhadi MT, Parvizi Mashhadi M, Nooghabi MJ, Hassanpour M, Abdollahi A. Iatrogenic injuries of the extrahepatic biliary system. The Journal of Surgical Research. 2017; 213 :215-221. DOI: 10.1016/j.jss.2015.11.032 - 74.
Ismael HN, Cox S, Cooper A, Narula N, Aloia T. The morbidity and mortality of hepaticojejunostomies for complex bile duct injuries: A multi-institutional analysis of risk factors and outcomes using NSQIP. HPB: The Official Journal of the International Hepato Pancreato Biliary Association. 2017; 19 (4):352-358. DOI: 10.1016/j.hpb.2016.12.004 - 75.
Strasberg SM, Helton WS. An analytical review of vasculobiliary injury in laparoscopic and open cholecystectomy. HPB (Oxford). 2011; 13 (1):1-14. DOI: 10.1111/j.1477-2574.2010.00225.x - 76.
de Santibañes E, Palavecino M, Ardiles V, Pekolj J. Bile duct injuries: Management of late complications. Surgical Endoscopy. 2006; 20 (11):1648-1653. DOI: 10.1007/s00464-006-0491-8 - 77.
Strasberg SM, Gouma DJ. 'Extreme' vasculobiliary injuries: Association with fundus-down cholecystectomy in severely inflamed gallbladders. HPB (Oxford). 2012; 14 (1):1-8. DOI: 10.1111/j.1477-2574.2011.00393.x - 78.
Truant S, Boleslawski E, Lebuffe G, Sergent G, Pruvot FR. Hepatic resection for post-cholecystectomy bile duct injuries: A literature review. HPB: The Official Journal of the International Hepato Pancreato Biliary Association. 2010; 12 (5):334-341. DOI: 10.1111/j.1477-2574.2010.00172.x