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Current Problems in Surgery 54 (2017) 406435

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Current Problems in Surgery

journal homepage: www.elsevier.com/locate/cpsurg

Diagnosis and management of biliary injuries


J. Bart Rose, MD, MAS, William G. Hawkins, MD*

Introduction

The diseases of the biliary tract are some of the most well described and complex problems
affecting human health. The importance of the biliary system has been recognized as far back as
Hippocrates when he classied bile as 1 of the 4 essential humors. Although our understanding
of anatomy and physiology has improved over the millennia, the effect of biliary disease on
mankind has not changed. More than 750,000 cholecystectomies are performed in the United
States each year. These operations, while extremely safe and effective, are not without risk. In
this monograph, we summarize the current knowledge surrounding bile duct injuries, including
the history of biliary surgery, the diagnosis of biliary injuries, the treatment of these injuries, and
techniques for prevention of biliary injury.

A brief history of biliary surgery

Laparoscopic cholecystectomy is the most common general surgical procedure performed in


the United States, with an estimated 90% of cholecystectomies performed in this manner.1 This
was not always the case.2 Although the rst account of human gallstones was in 1420 by the
Italian pathologist Antonio Benivieni.3 Two hundred years later in 1658 Francis Glisson was the
rst to ascribe gallstones to the clinical condition of biliary colic.4 This connection between
gallstones and biliary colic was indeed an advancement; however, the treatment of the disease
was another century away. In 1743, the French surgeon, Jean-Louis Petit, was able to successfully
treat acute cholecystitis by the creation of a percutaneous stula and removal of gallstones. His
technique relied on the opposition of an inamed gallbladder to the abdominal wall, thereby
limiting its generalized applicability.5 To work around this shortcoming, Dr. J. L. W. Thudichum
proposed a 2-stage procedure in which the gallbladder was sewn to the abdominal wall via a

From the Section of Hepatobiliary, Pancreatic, & Gastrointestinal Surgery, Department of Surgery, Washington University
School of Medicine, St. Louis, MO
n
Address reprint requests to William G. Hawkins, MD, Section of Hepatobiliary, Pancreatic, & Gastrointestinal Surgery,
Department of Surgery, Washington University School of Medicine, 660 S. Euclid Ave, Campus Box 8109, St. Louis, MO
63110.
E-mail address: hawkinsw@wustl.edu (W.G. Hawkins).

http://dx.doi.org/10.1067/j.cpsurg.2017.06.001
0011-3840/& 2017 Elsevier Inc. All rights reserved.
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 407

small transabdominal incision. Then several days later the gallbladder could be accessed
percutaneously without contaminating the peritoneal cavity.6 The rst attempt at surgical
removal of gallstones was performed on July 15, 1867 by Dr. John Stough Bobbs in Indianapolis,
Indiana. The case involved a 30-year-old woman with a 4-year history of biliary colic. On surgical
exploration of her abdomen Dr. Bobbs found an inamed gallbladder and performed a
cholecystotomy with removal of gallstones and reconstitution of the gallbladder. The patient
recovered and lived out the remainder of her life.7 In 1878, Dr. Marion Sims performed the rst
cholecystostomy in a single stage using the antiseptic techniques of Dr. Joseph Lister. He
performed a laparotomy, removed multiple stones through a cholecystotomy, and then sutured
the open gallbladder to the corner of the abdominal incision. Unfortunately, his patient died on
the eighth postoperative day due to hemorrhage.8 Dr. Theodor Kocher performed the rst
successful single stage cholecystostomy in June of the same year.9 Over time, these operations
remained focused on relieving symptoms and became more successful. However, it took time
before the underlying disease processes was more fully understood and treatments were altered
to address the disease.
Four years after Drs. Kocher and Sims performed the rst cholecystostomies, Dr. Carl Johan
August Langenbuch of Berlin performed the rst open cholecystectomy on July 15, 1882 with the
expressed intention of preventing future episodes of biliary colic by eliminating the source of the
gallstones. The following day his patient was afebrile, pain free, and smoking a cigar. He was able
to discharge to his home after 6 weeks.10 It took nearly 2 decades following Dr. Langenbuchs
rst cholecystectomy for it to surpass cholecystostomy as the treatment for biliary colic.
Dr. Langenbuchs technique remained relatively unchanged for more than 100 years before the
next major advancement in the surgical treatment of gallstone disease occurred.11
In 1982, a German gynecologist and engineer, Dr. Kurt Semm, performed the rst
laparoscopic appendectomy.12 This advancement in general surgery caught the attention of
fellow German surgeon, Erich Mhe, who postulated similar techniques could be applied to
removal of the gallbladder. Over the next 3 years he worked closely with Hans Frost, of the
German Manufacturing Company WISAP, on the development of a unique laparoscope which he
called the Galloscope (Fig 1). This device was a complex with instrument channels, a light
conductor, a duct to establish pneumoperitoneum, and side-viewing optics.13 Using this device
on September 12, 1985 Dr. Mhe performed the rst laparoscopic cholecystectomy using an
umbilical incision and 2 suprapubic working ports. The case took 2 hours and the patient
recovered quickly. Dr. Mhe began to modify his technique, and for his subsequent operations he
stopped using pneumoperitoneum and moved his working ports directly under the costal
margin. In fact, of the 94 laparoscopic cholecystectomies is in his initial series only the rst
6 were performed with pneumoperitoneum and working ports. The remainder was performed
through a single incision without pneumoperitoneum, and most without optical guidance. His
initial reports were met with skepticism.14 In March, 1987, French surgeon, Dr. Philippe Mouret,
performed a laparoscopic cholecystectomy during a joint gynecologic case. His case took 2 and a
half hours, and as there was no video available at that time, the procedure required him to lay
across the patients thigh and peer through the laparoscope while controlling instruments
inserted directly through the abdominal wall. The patient recovered well and subsequently
threatened to leave the hospital against medical advice on the rst postoperative day as she was
angered by the belief that her gallbladder could not possibly have been removed through such
small incisions.15 Dr. Mourets new laparoscopic cholecystectomy technique was subsequently
replicated by 2 other French surgeons Drs. Franois DuBois and Jacques Perissat.16 These French
surgeons were able to successfully publish their results and initially were given credit for the
development of the laparoscopic cholecystectomy as Dr. Mhe was unsuccessful in publishing
his results due to signicant language barriers. It was not until 1992 that Dr. Mhe nally
received recognition for his seminal work.17
Although there have been many attempts at advancement of the laparoscopic approach,
there have been no convincing data to suggest any of these techniques improve upon traditional
approaches. Single-incision laparoscopic surgery described rst by Dr. Giuseppe Navarra, of Italy,
has shown no benet over standard laparoscopy in multiple small randomized trials, with
408 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

Fig. 1. The original Galloscope developed by Dr. Erich Mhe. (Reprinted with Opensource permission from Reynolds.13)

increased operative time and cost.18-25 The most touted benet of single-incision laparoscopic
surgery is the cosmetic result; however, this too has been questioned in a recent randomized
control trial.26 The robotic cholecystectomy was rst successfully performed by Drs. Jacques
Himpens and Guy-Bernard Cadiere of Brussels, but accumulated data have led the Society of
American Gastrointestinal and Endoscopic Surgeons (SAGES) to state in their consensus
guidelines that there is no role for robotic cholecystectomy outside of training purposes due to
increased cost and no obvious benet.27 Natural orice cholecystectomy was rst described by
Ricardo Zorron of Brazil, and is a promising technique with early data suggesting it may be
comparable to laparoscopic surgery with improvements in pain and cosmesis.28 However, this
technique is not performed outside of a few centers, has limited long-term follow-up, and the
most common transvaginal approach is applicable in only one half of the population. These
authors strongly advocate that any future innovative surgical techniques be enrolled in
mandatory registries to evaluate for safety and participate in clinical trials to evaluate for
effectiveness.29
Shortly after the rst cholecystectomy came the rst biliary injury and in the early days of
biliary surgery these complications were common.30 The inexperience of the surgeons and the
advanced inammation present at the time of surgery surely contributed. These injuries created
the need for new techniques to surgically decompress or reconstruct the biliary system. In 1870,
Dr. Johann Nepomuk Ritter von Nussbaum of Germany is credited with suggesting that a surgical
anastomosis between the gallbladder and alimentary tract could be used to decompress an
obstructed biliary system.31 This was rst attempted by Dr. Alexander von Winiwarter in 1880,
where he sutured the gallbladder to the adjacent transverse colon, externalized this structure,
and 4 days later placed a fenestrated trocar through the gallbladder into the colon thereby
creating a cholecystocolotomy. The trocar was removed 8 days later and unfortunately resulted
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 409

in the formation of a biliary cutaneous stula. The initial colonic anastomosis was eventually
taken down and replaced with a loop of small bowel. The patient ultimately underwent
6 operations over the course of 12 years before his cutaneous stula nally resolved.32
Over the next decade there were many advances in the creation of biliary anastomoses. In
1887, Russian surgeon, Dr. Nestor Dmitrievic Monastyrski, successfully performed the rst single
stage cholecystojejunostomy for the treatment of metastatic periampullary carcinoma.33 The use
of a cholecystoduodenostomy for the treatment of biliary obstruction was rst successfully
completed by French surgeon Dr. Louis-Flix Terrier, and was performed over a 4 cm rubber
tube. This was also the rst use of an internal stent to aid in the construction of an
anastomosis.34,35 In 1892, Dr. Robert Gersuny became the rst to perform a cholecystogas-
trostomy for the treatment of an obstructed common bile duct.36,37 By 1894, the decompression
of the biliary system via cholecystoenterostomy was an accepted treatment for biliary
obstruction or persistent biliary stula. However, as cholecystectomy became more popular,
the use of the gallbladder for decompression was no longer a viable option and additional
techniques were required. The rst side-to-side choledochoduodenostomy was performed by
Dr. Oskar Sprengel in 1891, in Dresden Germany.38 In 1898, Dr. William Stewart Halsted
performed the rst end-to-side choledochoduodenostomy following the resection of a
periampullary cancer.39 As surgical techniques evolved, and surgeons began addressing more
proximal biliary strictures and cancers, it became necessary to perform higher level
anastomoses. The rst end-to-side hepaticoduodenostomy was performed by Dr. Hans Kehr of
Germany in 1902 for the treatment of an extrahepatic cholangiocarcinoma.40 In 1904,
Dr. Ambrose Monprot of France used Dr. Cesar Rouxs Y anastomosis to create a
cholecystojejunostomy in an effort to reduce tension on the anastomoses and reduce reux of
intestinal contents into the biliary system causing cholangitis.41 This technique was later
improved upon by Dr. Robert Dahl of Sweden who performed the rst Roux-en-Y
hepaticojejunostomy in 1909.42 To address hilar injuries and malignancies, it became necessary
to develop techniques to reconstruct the biliary tree in the absence of viable extrahepatic ducts.
Dr. William Longmire of the United States addressed this in 1948 by resecting a portion of the
left liver and creating an intrahepatic cholangiojejunostomy.43 In 1956, Drs. Jacques Hepp and
Claude Couinaud of France showed that by using the long extrahepatic portion of the left hepatic
duct as the anastomotic site for a side-to-side Roux-en-Y hepaticojejunostomy, a liver resection
could often be avoided.44 However, this approach was not very benecial for complex biliary
injuries above the conuence as the right ductal system was often in discontinuity. In 2000,
Dr. Steven Strasberg of the United States described a method using a modied Hepp-Couinaud
technique and percutaneous transhepatic biliary stents to locate the right ductal system
intrahepatically and performed a Roux-en-Y hepaticojejunostomy for reconstruction.45 Key
moments in the advancement of biliary surgery are depicted in the timeline shown in Fig 2.

Incidence of biliary injury

Although the rate of severe biliary injury was accepted to be less than 0.3% in the era of open
cholecystectomy, this increased to as high as 1.5% in the early laparoscopic experience.46-50 As
surgeons have become more experienced with laparoscopic surgery, and improving technology
has allowed for better visualization, modern series report a population-based incidence of
0.08% to 0.12% for severe injuries and a rate of 1.5% for all injuries.51,52

Risk factors for biliary injury

The rate of biliary injury was initially associated with a learning curve effect. As
laparoscopic cholecystectomy has supplanted open cholecystectomy as the most common
approach, this operator inexperience is thought to contribute less to the current rate of
410 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

Fig. 2. Timeline depicting key moments in biliary surgery. (Photo of Claude Couinaud reprinted with permission from
McClusky DA, Skandalakis LJ, Colborn GL, Skandalakis JE. Hepatic surgery and hepatic surgical anatomy: Historical
partners in progress. World J Surg. 1997;21(3):330-42, Springer.)

injuries.53,54 There are a number of risk factors that make cholecystectomy more challenging.
These factors can be patient related, disease related, or extrinsic.55

Patient-related factors

Patient-related factors include aberrant anatomy, male sex with associated larger anterior
posterior abdominal diameter, prior operations, and advanced age.56 Obesity and skeletal
deformities can make exposure more challenging. Steatotic livers can be stiff and, fragile, or both
and may limit retraction and visualization. Intrahepatic gallbladders can limit the ability of the
surgeon to apply appropriate tension on the cystic duct and lead to inadequate exposure.
Congenital abnormalities can be associated with aberrant cystic duct insertions and make
identication of key structures difcult. Aberrant anatomy is a well described risk factor for
biliary injury, with an aberrant right hepatic duct being the most common anomaly associated
with injury. Injuries to these aberrant right ducts may go underreported because they can be
asymptomatic.57-59 However, it is important to note that most bile duct injuries occur in the
setting of standard biliary anatomy.
Many surgeons attribute small postoperative bile leaks to transection of small bile ducts
draining directly into the gallbladder, the so-called ducts of Luschka, but this is incorrect. In
1863, while the German anatomist Hubert von Luschka did describe a microscopic network of
ducts within the soft tissue surrounding the gallbladder, these ducts were present on the entire
surfaces of the organ, and likely represented lymphatic channels. What modern surgeons are
attempting to describe are more accurately called subvesicular bile ducts. In a 2012 systematic
review of the literature this anomaly had a prevalence of 4%, a mean diameter of 2 mm, drained
primarily into the right hepatic ductal system, and manifested as 4 distinct subtypes (Fig 3).
Subtypes 1 and 2 represent replaced or accessory right posterior sectional ducts, respectively,
and run posterior to the cystic plate. These are likely the most common subtypes and can be
injured if the surgeon is below the cystic plate. Subtype 3 is a hepaticocholecystic duct draining
bile from the right ductal system directly into the gallbladder and subtype 4 involves a network
of small bile ducts within the connective tissue of the gallbladder fossa; both are likely rare.60
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 411

Fig. 3. Types of subvesical bile ducts: type 1segmental or sectorial subvesical bile duct, type 2accessory subvesical
bile duct, type 3hepaticocholecystic bile duct, type 4aberrant subvesical bile duct. (Reprinted with permission from
Schnelldorfer and colleagues,60 Springer.)

The rarity of subtypes 3 and 4 can potentially be explained by embryology. The primitive
gallbladder develops as a diverticulum arising from the liver primordium. The cranial portion of
the liver primordium will develop into hepatic cords and eventually the future liver. The
gallbladder diverticulum will develop caudal to this and fuse to the liver by the third month of
gestation. Since these structures develop separately, it should be rare to have a ductal connection
directly between them.61

Disease-related factors

Disease-related risk factors include severity of inammation, hemorrhage, and presence of


abscess. The presence of acute cholecystitis has been associated with a 2- to 3-fold higher rate of
biliary injury when compared to elective cases.62 Impacted large gallstones, Mirizzis syndrome,
or stulae to adjacent organs can all cause obliteration of standard surgical planes, making
dissection difcult and, on occasion, impossible.

Extrinsic factors

Examples of extrinsic factors increasing the risk include equipment failure, operating room
(OR) distractions, and tness or training level of operative personnel.63 Clips can slip off or be
placed too proximally onto the common bile duct, causing subsequent structuring. Inadvertent
thermal injury to the common bile duct may not cause immediate injury but can result in
delayed stricturing. Breakdown of insulation on laparoscopic equipment can lead to unintended
electrical arcing and subsequent injury to adjacent tissues.

Avoidance of bile duct injury in cholecystectomy

To avoid biliary injury, 5 methods of identifying cystic structures during cholecystectomy


have been widely described and they are as follows50,64,65: (1) infundibular technique, (2)
dissection of the common bile duct to ensure the cystic duct insertion is identied, (3) critical
view of safety (CVS), (4) intraoperative cholangiography, and (5) use of advanced imaging
techniques.
412 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

Fig. 4. (A) The usual anatomy when the infundibular technique is applied. The cystic duct-gallbladder junction is
characterized by a aring tunnel shape (bold lines). Arrow represents circumferential dissection of the common duct
(CD)-gallbladder junction during the infundibular technique. (B) Inammation can pull the common bile duct (CBD)
onto the gallbladder creating a similar aring tunnel shape. As a result, the CBD is mistaken for the cystic duct, resulting
in classic injuries. CHD, common hepatic duct. (Reprinted with permission from Strasberg S. Error traps and vasculo-
biliary injury in laparoscopic and open cholecystectomy. J Hepatobiliary Pancreat Surg 2008;15(3):285, Elsevier.)

Infundibular technique

Infundibular technique involves dissection around of the lower portion of the gallbladder to
identify the cystic duct. The infundibular technique is limited in utility for severely inamed
gallbladders and those with large effacing stones. In these situations the infundibulum and
common duct can become fused, and as the surgeon approaches the infundibulum the common
duct may be mistaken for the cystic duct and transected inadvertently. As the dissection is
carried up along the suspected medial edge of the gallbladder, a second tubular structure is then
encountered, often after transection, at which point the surgeon realizes a bile duct injury has
occurred. This is known as the classic injury and is depicted in Fig 4.53

Common duct dissection

Skeletonization of the common hepatic or bile duct has been suggested as a method to
identify the cystic duct. However, this technique needlessly places these structures or aberrant
biliary structures (eg, low inserting right hepatic or posterior sectional ducts or an anterior
coursing right hepatic artery) at risk for injury.

Critical view of safety

Beginning in 1995, Dr. Strasberg and colleagues50,66 have been promoting the The Critical
View of Safety to help avoid the error of misidentication contributing to biliary injury. The CVS
has the following 3 principal requirements: (1) the triangle of Calot be cleared of all fat but does
not require the common bile duct to be exposed, (2) the gallbladder infundibulum be separated
from the cystic plate, and (3) before anything is divided it should be clear that 2, and only 2,
structures should be seen entering the gallbladder as depicted in Fig 5. It is imperative to
understand that the CVS has not been obtained until all 3 of these requirements are met. It is not
adequate to create 2 windows between the cystic duct, cystic artery, and base of the liver
without clearly delineating the cystic plate. The difference between a 2 window view and the
CVS is shown in Fig 6. If the cystic plate is not exposed, the surgeon cannot be certain that
the common hepatic duct, or aberrant right bile duct, are not adherent to the posterior surface of
the gallbladder. Once the CVS is obtained, this view should be documented within the operative
note and ideally by a doublet digital photograph from both a medial and lateral vantage point.67
If this view cannot be obtained, there are several safe options (see below) for subtotal
cholecystectomy. The results of the CVS technique have been evaluated in a large retrospective
study and determined that the observed-to-expected ratio of major bile duct injuries over a
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 413

Fig. 5. The critical view of safety. The triangle of Calot has been dissected free of fat and brous tissue; however, the
common bile duct has not been displayed. The base of the gallbladder has been dissected off the cystic plate and the
cystic plate can be clearly seen. Two and only 2 structures enter the gallbladder and these can be seen circumferentially.
(Reprinted with permission from Strasberg and Brunt,66 Elsevier.)

5-year period had improved by an order of magnitude since adopting the CVS technique.68
A video teaching program of this technique and others surrounding the culture of safety has
been devised by its creator and is available for viewing online.69

Intraoperative cholangiography

Routine use of intraoperative cholangiography has not been shown to have denitive
benet in any prospective randomized trial. Several large retrospective studies have
suggested that the incidence of biliary injury is lower in patients with intraoperative
cholangiography performed.47,70 Intraoperative cholangiography does not in itself prevent
bile duct injury, but may be useful in delineating anatomical ambiguity and preventing
severe injury.71 The cost-effectiveness of this approach is questionable.72 Intraoperative
cholangiography can be falsely reassuring in situations of aberrant right posterior sectional
duct insertion in which the cholangiography can appear normal to an inexperienced surgeon
(Fig 7).

Fig. 6. Difference between creation of 2 windows and obtaining the critical view of safety (CVS). (A) Dissection has
led to the creation of 2 windows. The rst window is between the cystic duct and artery and the second between the
cystic artery and the liver. This does not fulll criteria for a CVS as the cystic plate cannot be clearly identied. (B) Critical
view of safety is obtained with a well-dened cystic plate. (Color version of gure is available online.)
414 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

Fig. 7. (A) Endoscopic retrograde cholangiopancreatography image showing a right aberrant duct from segment 5. The
cystic duct enters the aberrant duct near the clips (arrow). (B) Reconstruction of the image of what a cholangiography
would look like if the aberrant duct was cannulated. Few surgeons would realize that one segmental duct is missing and
that an injury to the right aberrant duct has occurred. (C) Reconstruction of the image of what a cholangiography would
look like if the right main hepatic bile duct was cannulated. Note the much more obvious absence of the right hepatic
ducts. The arrow points to the left hepatic duct. (Reprinted with permission from Strasberg,65 Elsevier.)

Advanced imaging techniques

Intraoperative ultrasound
The routine use of intraoperative laparoscopic ultrasound may decrease the incidence of bile
duct injury as suggested by a large multicenter trial wherein 1300 patients at 5 institutions
underwent laparoscopic cholecystectomy without a major bile duct injury being observed.73
However, a standardized technique for laparoscopic cholecystectomy was not described and
more than one third of the patients had concomitant intraoperative cholangiography.
Intraoperative ultrasound may be best used for evaluation of choledocholithiasis, and not as a
routine technique to avoid biliary injury. A recent meta-analysis comparing intraoperative
ultrasound to intraoperative cholangiography found ultrasound to be as effective in diagnosing
choledocholithiasis, but with less expense, a lower failure rate, and no exposure to ionizing
radiation for the patient and staff.74

Near-infrared imaging
One of the more contemporary techniques being investigated to reduce bile duct injury
during cholecystectomy is the use of indocyanine green and near-infrared light to directly
visualize the biliary system and cystic artery. Indocyanine green is a uorescent molecule that is
administered intravenously and binds to plasma proteins. It reaches a peak arterial concentration
1-2 minutes after injection. It is primarily excreted in bile and will reach a peak biliary
concentration between 30 minutes and 2 hours after administration. When exposed to near-
infrared light with a 700-800 nm wavelength it will excite and emit uorescence between 750 and
950 nm. This can be detected with specialized laparoscopic cameras and will help identify vascular
and biliary structures. Current evidence for its use is limited, but a recent meta-analysis suggests it
holds a slight advantage over inversion of control for identifying the cystic duct, with a relative risk
of 1.16, but had no advantage in identifying the common or hepatic ducts.75

Strategies to avoid biliary injury if the cystic duct cannot be identied

If the cystic duct cannot be identied with certainty by 1 of the above approaches, then 1 of
the following 3 approaches should be taken. First the operation can be aborted and the patient
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 415

Fig. 8. Subtypes of subtotal cholecystectomy. (A) The fenestrating subtype leaves the gallbladder open after removal of
the free, peritonealized portion of the gallbladder wall. The cystic duct orice can be sutured closed (inset) or left open
and a drain placed. (B) The reconstituting subtype recreates an intact lumen to prevent leak, but allows for future stone
formation. (Reprinted with modication from Strasberg and colleagues,76 Elsevier.)

can be referred to a hepatobiliary specialist. Alternatively, a cholecystostomy tube can be placed


as a temporizing measure and the operation attempted again in 4-6 weeks. Or lastly, a subtotal
cholecystectomy can be performed in either a fenestrating or reconstituting manner.76 With the
fenestrating subtype, the free peritonealized wall of the gallbladder is removed down to a lip of
tissue at the lowest portion which serves as a shield to protect inadvertent injury to adjacent
structures. The stones are then extracted, the mucosa is ablated, and the cystic duct orice is
either oversewn with a pursestring or a drain is placed (Fig 8). The reconstituting subtype is
essentially the same as above, but instead of leaving the gallbladder open, the remaining
gallbladder wall is closed (Fig 8). These authors prefer the fenestrating subtype to limit the
chance of future stone formation.

Diagnosis of suspected biliary injury

Even with careful planning and adherence to safe surgical techniques, a bile duct injury can
occur. Accurate identication of the extent of injury is imperative to ensuring proper operative
planning and ensuring a durable repair. Less than one third of biliary injuries are recognized at
the time of the index operation.77,78 These injuries are discovered at the time of surgery either
by direct visualization of a leak or on intraoperative cholangiography. Once a biliary injury is
suspected, it is important to determine the existence and degree of any associated vascular
injury. Concomitant vascular injury occurs in 12% to 61% of biliary injury cases and will involve
the right hepatic artery or its branches 90% of the time.46,79-81 Identication of vascular injury is
necessary to determine if early repair is possible, as biliary ischemia signicantly increases the
risk of delayed stricturing.
Unfortunately, most biliary injuries are not recognized immediately and manifest in a delayed
fashion. Biliary injuries can be categorized into 2 main groups, leaks or obstruction, which can
manifest concurrently. Patients with leaks generally have symptoms within 3 days whereas
those with an obstruction present in a delayed manner.82 Hepatic bile has a low concentration of
bile acids and therefore is unlikely to cause extreme peritoneal irritation; unlike gallbladder bile
in which bile salts can be concentrated up to 20-fold and can cause abdominal discomfort. There
is still some controversy as to the exact mechanism separating bile ascites from bile peritonitis,
but bile acid concentrations and bacterial colonization seem to play a role.83 Therefore, patients
416 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

with main duct leaks typically present with nonspecic, occasionally transient, abdominal
symptoms such as fullness, nausea, vomiting, pain, distention, fevers, or chills. Delays in
diagnosis may lead to a biliary stula, cholangitis, sepsis, biloma, abscess, and multisystem organ
failure.84 To further complicate the matter, liver function tests may be normal or only mildly
elevated. In the absence of signicant laboratory abnormality, imaging is often required to make
a diagnosis of biliary injury.
Patients with biliary obstruction typically present with vague abdominal symptoms,
jaundice, liver enzyme elevation, and anorexia. Liver enzyme elevation alone does not accurately
predict complication, as it may be falsely elevated transiently due to an unknown mechanism
related to pneumoperitoneum.85-87 This transient elevation will generally resolve after 1 week
but may be responsible for delaying the diagnosis of true biliary injury.77 Thermal injury to the
common duct may manifest as delayed stricturing weeks to months later, and can be associated
with recurrent cholangitis, obstructive jaundice, or secondary biliary cirrhosis.84
No injury should be repaired if the surgeon lacks the required expertise.65 Most general
surgeons are capable of repairing minor injuries such as cystic duct leaks or partial duct
lacerations. However, more complex injuries have been shown to have better outcomes when
repaired in the hands of experienced hepatobiliary surgeons.88-90 The success rate of bile duct
injury repair in hepatobiliary surgeons hands versus the primary surgeon is signicantly higher
(79% vs 27%).56,77 Despite this drastic difference in outcomes, up to 75% of repairs are still
attempted by the primary surgeon.56 If an injury occurs at an institution that lacks the expertise
for repair, it is recommended that the surgical bed be widely drained and the patient referred to
a tertiary care center. Centers that do not routinely treat biliary injuries should generally not
attempt further treatments (eg, endoscopic retrograde cholangiopancreatoscopy [ERCP]) as
nearly one half of interventions performed may be inappropriate.89 Delays in referral have been
associated with increased complication rates and mortality rates.84,89,90

Initial evaluation of suspected biliary injury

Initial radiographic imaging should be directed toward conrming the presence of a bile duct
injury, which is commonly accomplished with either an ultrasound or computed tomography
(CT). Both are adequate for diagnosing obstruction by showing biliary ductal dilatation, but will
be unable to distinguish an intra-abdominal uid collection between a seroma, lymphocele,
hematoma, or biloma. Small uid collections in the gallbladder fossa are common and occur in
10%-14% of patients after cholecystectomy.91-93 These small collections are usually asymptomatic
and clinically irrelevant. Large uid collections outside of the gallbladder fossa raise concern for
injury.
The next step in evaluation of a suspected leak is to conrm the presence of bile in the uid
collection via percutaneous sampling of the uid collection or hepatobiliary iminodiacetic acid
scintigraphy. Aspiration has the advantage of being both diagnostic and therapeutic. It is
important to evacuate intra-abdominal contamination before the development of an abscess,
sepsis, or multisystem organ failure. The earlier this can be done, the lower the chance
subsequent infection.78 Although a hepatobiliary iminodiacetic acid (HIDA) scintigraphy scan
may show evidence of extrahepatic bile, it will not identify the specic location of that leak or
clarify the extent of injury, and is rarely used today. Our practice is to perform aspiration of
suspected uid if clinically worrisome for leak.
Once a biliary injury is conrmed, the extent of injury must be evaluated. The gold standard
for identifying and evaluating bile duct injuries is cholangiography by either percutaneous
transhepatic, endoscopic, or magnetic resonance (MR) methodology. Each of these modalities
has distinct advantages and disadvantages.
ERCP can provide very accurate determination of the level and extent of biliary injury. Once
an injury is identied, this technique has advantage of allowing for direct therapeutic
intervention. Sphincterotomy and stent placement can decrease the pressure gradient within
the biliary system and allow for increased rates of healing. Covered stents may be used to bridge
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 417

Fig. 9. Strasberg type E3 injury with occlusion at the level of the hilum. U-tube placed into right posterior sectional duct
and exiting liver at separate site.

defects, allow for reduced healing times, and decrease future stricture rates.94 However, an ERCP
cannot visualize proximal ducts if a branch has been occluded with a clip or ligature. Although
generally quite safe, endoscopic interventions do carry with them their own risks, including
perforation, postprocedural pancreatitis, hemorrhage, sepsis, cholangitis, and death.
If the suspected injury involves a ductal occlusion, or a prior ERCP could not adequately
visualize proximal ducts, then a percutaneous transhepatic cholangiography should be
considered. With this procedure, a dilated proximal bile duct is cannulated percutaneously
under radiographic guidance and then injected with contrast to conrm leak or occlusion.
Various therapeutic interventions may also be performed via percutaneous transhepatic
cholangiography, such as drainage, stenting, or serial dilations of delayed strictures. This
modality is the most invasive and complications including bleeding, cholangitis, or further
biliary injury can occur at rates approaching 7%.95
Magnetic resonance cholangiopancreatography (MRCP) provides a noninvasive way to
evaluate the proximal and distal biliary system for injury. Additionally, some information on
vascular anatomy can be obtained. MRCP can often provide very detailed anatomical information
beyond that obtained by cholangiography, allowing for better preoperative planning.96,97
However, to obtain adequate images the patient must be able to cooperate and lay motionless
for a prolonged period with periodic breath holding. Failure to do this may result in poor image
quality.
It is our practice to attempt endoscopic stenting for distal injuries to the common hepatic
duct or cystic duct stump leaks. For more proximal injuries, such as those to the right posterior
ductal system, a percutaneous approach is usually favored. A percutaneous drain placed into the
injured biliary system that exits the liver parenchyma and returns through the abdominal wall in
a separate site creating a U-shaped drainage system is our preferred method for draining these
proximal injuries with concomitant leak (Fig 9). This system has the advantage of
decompressing the proximal biliary system and draining extrahepatic uid collections with
the same drainage tube, while being very secure and limiting the chances of accidental removal.

Vascular injury

The initial workup should include thorough evaluation of the hepatic vascular system to
evaluate for concomitant injury. Vascular injuries may be evaluated by ultrasound duplex, MRCP
with angiography, or computed tomography angiography. The rate of vascular injury at the time
of bile duct injury is estimated to be between 7% and 32%.46,98 The right hepatic artery is the
most likely to be injured given its proximity to the gallbladder and that it is the supplying vessel
418 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

Fig. 10. Effect on hepatic blood ow of an injury to the right hepatic artery (RHA) without biliary injury. (A) Occlusion of
the RHA results in ischemia of the right liver, but (B and C) ow is restored by preformed collateral arterial shunts.
(Reprinted with permission from Strasberg and Helton,79 Elsevier.) (Color version of gure is available online.)

to the cystic artery. In severely inamed gallbladders the cystic artery can be fused with the right
hepatic artery, leading to signicant injury. Injury to the hepatic artery will rarely produce
signicant ischemia in the right liver due to the portal blood supply and shunting via the
transverse hilar marginal artery and marginal bile duct arteries (Fig 10). Vascular injury in the
hilum can be associated with signicant liver injury by disrupting these shunts and can cause
hepatic necrosis, intrahepatic abscess, or liver atrophy. Extreme vasculobiliary injuries can
involve major hepatic arteries and portal veins. These extreme injuries may require major liver
resection or transplantation to treat, and can carry a mortality rate of up to 50%.81,99-101 Although
isolated injury to the right hepatic artery may have limited effect on the liver, it is the primary
blood supply to the common hepatic bile duct and its transection may contribute to delayed bile
duct stricturing secondary to bile duct ischemia. Vasculobiliary injuries have been shown to
have higher rates of abscess formation, postoperative bile leaks, and anastomotic stricture
rates.102,103

Classication

Bismuth classication system

A number of classication systems have been proposed to describe biliary injuries or guide
treatment. The rst reported was the Bismuth system in 1982.104 This system categorizes
strictures based on anatomical level of injury. Type 1 strictures are located on the common
hepatic duct greater than 2 cm below the biliary conuence. Type 2 lesions are less than 2 cm
below the conuence involving the common hepatic duct. Type 3 lesions are strictures at, or
above, the conuence with intact communication between the left and right hepatic ducts. Type
4 lesions are similar to type 3, but the left and right hepatic ducts do not communicate. Type
5 strictures involve injury to the common hepatic duct and an aberrant right posterior sectional
duct. This classication system can help guide the surgeon as to the type of repair necessary
to address a specic injury.105 This classication system is disadvantaged in the fact that it
only describes strictures and not more complex injuries often seen with laparoscopic
cholecystectomies.

Strasberg classication system

To better describe injuries seen with laparoscopic cholecystectomies, Strasberg and


colleagues50 proposed expansion of the Bismuth classication system in 1995 (Fig 11). This
system can accurately describe the location of leak, full or partial transection, and complete
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 419

Fig. 11. Strasbergs classication of bile duct injuries. Strasberg type A injury is a cystic duct stump leak or minor hepatic
duct leak without loss of continuity of the biliary tree. Type B is an occlusion of an aberrant right duct. Type C is a
transaction of an aberrant right duct. Type D is a partial transection of the common hepatic duct encompassing less than
50% circumference of the duct. Type E injuries are analogous to the Bismuth system. (Reprinted with permission from
Strasberg and colleagues,50 Elsevier.)

occlusions. This system has the advantage of guiding operative repair based on level of injury,
but does not account for concomitant vascular injury.

Stewart-Way classication system

In 2003, Stewart and Way reported on a new classication system based on the mechanism
and anatomy of the injury (Fig 12).106 A class 1 injury refers to an incomplete transection of a bile
duct with no loss of tissue and represented 7% of the reported injuries in their series. This
occurred through 2 different mechanisms. The rst was misrecognition of the cystic duct and the
common duct with early recognition of injury and minimal loss of tissue. The second mechanism
occurs through lateral injury of the common hepatic duct resulting from extension of a cystic
ductotomy for cholangiography. A class 2 injury is a lateral injury to the common hepatic duct
420 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

Fig. 12. Stewart and Way classication: the mechanism of the injury is in the text. Class III injuries are subdivided
according to the location of the proximal line of transection. (Reprinted with permission from Way and colleagues,106
Lippincott Williams & Wilkins.)

that results in stenosis. It is often the result of thermal damage or clamping of the duct
inadvertently. It occurs in 2% of biliary injury cases. Class 3 injury represents complete
transaction of the common hepatic duct and is the most common injury, occurring in 61% of
cases. Class 3 injuries are further subdivided into the following 4 subtypes: subtype A, in which
there is a remnant common hepatic duct; subtype B, which describes transection at the level of
the biliary conuence; subtype C, which describes a loss of the biliary conuence; and subtype
D, which describes injuries above the biliary conuence with transection of secondary biliary
radicals. Type 3 injuries are associated with the mistaken identication of the common hepatic
duct as the cystic duct. This leads to complete transection and excision of a segment of the
common hepatic duct during extirpation of the gallbladder. In 20% of these cases the proximal
hepatic duct was clipped; in the remaining 80% the transected duct was left open and the patient
developed bile ascites. Type 3 injuries are associated with a concomitant vascular injury in 27%
of cases. Finally, class 4 injuries are to a right or aberrant right hepatic duct with concomitant
injury of the right hepatic artery. Rarely will this involve concomitant injury to the conuence
(4% of cases). This injury occurs with a prevalence of 10%. This system is disadvantaged in that it
does not describe delayed injuries such as strictures or subcategorize higher injuries above the
conuence to aid in planning operative repair.

Neuhaus classication system

The Neuhaus system was published in 2000 to offer broader descriptions of injury than the
Strasberg system.107 The Neuhaus system has 5 main injury categories, each with 2 subcategories
with the exception of type E injuries with 4 subcategories. Type A1 injuries are cystic duct stump
leaks and A2 are bile leaks from the liver bed. Type B1 injuries are incomplete occlusions of the
common bile or hepatic ducts and a B2 is a complete occlusion. Type C1 injuries are lateral
injuries to the common or hepatic bile duct less than 5 mm in length while C2 are greater than
5 mm. Type D1 is a transection of the common or hepatic bile duct without structural defect,
while D2 includes a structural defect. Type E injuries describe stenoses of the common or
hepatic bile duct. Type E1 injuries are common bile duct injuries with a stenosis less than 5 mm
in length. E2 injuries have common bile duct stenoses greater than 5 mm in length. E3 stenoses
are at the conuence, while E4 stenoses are in the right hepatic duct or segmental ducts.

Hanover classication systems

The Hanover system, published in 2007, expanded on the Neuhaus system by adding further
subcategories of injuries and including vascular injuries (Fig 13).108 The Neuhaus type C and D
injuries gained 2 further subcategories to describe lesions at the hepatic bifurcation or above the
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 421

Fig. 13. Neuhaus system. This system expanded on the Strasberg system by adding new subcategories. CBD, common
bile duct. (Reprinted with permission from Schmidt and colleagues,102 Springer.)
422 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

hepatic bifurcation, with modiers to describe various vascular injuries. For example, a
transection at the level of the hepatic bifurcation with a right hepatic artery injury would be
classied as a Hanover D3d injury. The Hanover classication is extremely descriptive, but due to
its complexity it is hard to use in a clinical setting and may be more appropriate for accurate
academic reporting rather than guiding clinical decision-making.
Multiple other classication systems have been described but have not gained widespread
acceptance.109,110 Regardless of the system used, it must be applied in a consistent way if
accurate systematic reviews or meta-analyses are to be performed. A proposed system of tabular
reporting may be the most reliable way to achieve this and should be considered by any
investigator looking at a clinical problem with a low incidence.111

Management of bile duct injuries

Endoscopic management

The goal of endoscopic management of biliary injuries is to reduce the pressure gradient
across the sphincter of Oddi and allow for preferential drainage of bile into the duodenum rather
than through an injury site.112 This is typically achieved via a combination of sphincterotomy
and placement of biliary endoprosthesis. Most cystic stump leaks or small lateral injuries to
aberrant right hepatic ducts can be managed successfully with this modality.113,114 However, for
injury sites other than these, endoscopic management may not be as effective.114 Complete
transection of a duct typically cannot be managed endoscopically as access to bile ducts proximal
to the site of injury is inaccessible. Patients must be informed that ERCP is not a benign
procedure and is associated with a 6.8% overall complication rate (eg, 3.5% pancreatitis, 1.3%
bleeding, and 0.6% perforation rates) and a 0.33% mortality rate.115

Surgical management

General concepts
Any planned anastomosis should be performed in a tension-free manner with a mucosa-to-
mucosa anastomosis using absorbable monolament sutures and should drain all segments of
the liver.45 Depending on the level of injury, the biliary tract can be reconstructed utilizing either
a Roux-en-Y jejunostomy or the adjacent duodenum. Both have been shown to be successful
even for Strasberg type E injuries.116 The duodenum should only be used if it is not inamed and
can be mobilized sufciently to insure a tension-free repair. If the duodenum is used in a side-to-
side fashion without a transection of the distal bile duct, then a sump syndrome can develop
with a theoretical risk of cholangitis. A direct duct-to-duct anastomosis is not recommended as it
is associated with a 50% failure rate and late stenosis. This is likely related to devascularization of
the bile ducts during circumferential mobilization.117,118

Incision
Data on minimally invasive bile duct repairs are limited to small case series and case reports.
The largest case series describing laparoscopic biliary reconstruction included 29 patients,
8 with injuries at or above the conuence, and only 1 stricture with 3-year follow-up.119 A single
case of robotic-assisted bile duct repair has been reported, but this modality has been applied
successfully to creating bilioenteric anastomoses for other hepatobiliary disease processes.120-123
Although these early results are promising, this approach is not widely accepted and we
recommend an open approach for any complex bile duct repair as adequate exposure is
necessary for successful repair. These authors prefer either a generous midline incision or a right
subcostal incision approximately 6 cm below the costal margin with a midline extension. In
obese patients this subcostal incision can be extended to the left, creating a Mercedes-Benz
type incision. The midline extension should be extended above the xiphisternum to maximize
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 423

Fig. 14. Bile duct anatomical variations: (A) common variations of the right biliary system and (B) common variations of
the left biliary system. (Reprinted with modication from Strasberg SM, Hawkins WG. Reconstruction of the bile duct. In:
Fischer J, editor. Mastery of Surgery. 5th ed. 2007. p. 1129-42, Lippincott Williams & Wilkins.)

rib retraction. A xed retractor, such as a Bookwalter or Thompson, is preferred to maintain


exposure. Surgical loupes are recommended for precise placement of the ne suture used in
these repairs.

Relevant anatomy
For any injury at or above the conuence, imaging should be obtained to evaluate for biliary
or arterial aberrancy that can complicate reconstruction. Two surgically important biliary
anomalies manifest on the right side of liver (Fig 14). The rst is an insertion of a right sectional
duct (the most common being the posterior sectional) into a left duct, which occurs with a
frequency of 20%. The next surgically relevant anomaly is a low insertion of the right posterior
424 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

Fig. 15. Blood supply to the bile ducts. Element 2: the marginal arteries. Marginal arteries are disposed at 3, 9 and, rarely,
12 oclock (not shown) on the common bile duct or common hepatic duct. The hilar marginal artery runs across the top
of the conuence of the right and left hepatic ducts. (Reprinted with permission from Strasberg and Helton,79 Elsevier.)
(Color version of gure is available online.)

bile duct below the level of the conuence. This can occur in approximately 2% of individuals,
and is a common cause of biliary injury associated with laparoscopic cholecystectomy. The
anatomically signicant variations of the left hepatic duct involve the variable insertion of the
segment 4 segmental duct (B4). Insertion of B4 close to the conuence may require
reconstruction at this level to include multiple anastomoses (Fig 14).
The blood supply to the bile ducts is derived from the hepatic arteries. It runs in an axial
fashion along the length of the bile duct. Superiorly the blood supply drives from branches of the
main or right hepatic artery and rarely from the left at the level of the conuence. These superior
branches will travel at the 3- and 9-oclock positions inferiorly where they form an anastomosis
with a blood supply derived from the gastroduodenal artery. Along the course of the main biliary
arteries are small longitudinal artery branches that will directly supply the bile duct. Depending
on the level of bile duct transaction, a watershed zone may be encountered between the inferior
and superior blood supplies. With injuries close to the conuence, the distal section of injured
bile duct may become ischemic, while injuries close to the level the duodenum may result in the
proximal injured bile duct developing ischemia (Fig 15). This becomes clinically relevant when
planning repair as an anastomosis closer to the biliary conuence will have the most robust
blood supply. This also reinforces the need to thoroughly investigate for concomitant vascular
injury as an early repair in the setting of a right hepatic artery injury may be associated with
biliary ischemia and worse anastomotic outcomes. Circumferential dissection of the bile duct
may injure posterior branches and therefore anastomosis to the anterior surface is considered
safer.

Timing of repair
The management of bile duct injuries varies depending on the degree of injury and the time
frame when the injury is rst discovered. This complication can be managed either
nonoperatively or operatively in an early or delayed fashion. All injuries must rst be adequately
characterized by the location, the degree of injury, and presence of concomitant vascular injury.
The experience of the operating team, the stability of the patient, the amount of acute
inammation, as well as the extent of vasculobiliary injury all play an important part in
determining the success of a repair.84,88 The timing of the repair does not affect the overall
anastomotic patency. However, patients who undergo repair after 1 week of injury, but before 6
weeks, have an increased risk of perioperative complication. 84,124,125 Signicant care should be
taken in planning any biliary repair as subsequent attempts will progressively become less
successful and more technically challenging.
Less than one third of biliary injuries are detected immediately at the time of
cholecystectomy. If this injury is minor, then an intraoperative repair may be attempted by
the index surgeon depending on his comfort level.65 Small leaks from the cystic duct stump can
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 425

be ligated laparoscopically or hand sewn. Small lateral injuries (Strasberg type D) can also be
repaired by experienced surgeons by closing the injury over a T-tube with small absorbable
monolament sutures. Alternatively, the injury can be repaired primarily using the same small
monolament, but instead of a T-tube, a small drain such as a pediatric feeding tube can be
placed into the cystic duct stump and utilized as the stent. These small lateral injuries can also
be managed endoscopically or with a percutaneous transhepatic biliary drainage (PTBD).
More complex injuries such as Strasberg type E injuries should only be repaired by
experienced hepatobiliary surgeons as they often require complex biliary bypass procedures. If a
hepatobiliary surgeon is unavailable at the time of the index operation, then the operative bed
should be irrigated, a drain should be placed near the injury, and the patient should be
transferred to a tertiary care center. Attempted repair of complex injuries by an inexperienced
surgeon should be avoided as it is associated with an 80% failure rate.88 With severe injuries
above the level of the biliary conuence, those patients with severe concomitant vascular injury,
or in the setting of severe inammation, a delayed repair is often advisable. Nearly one third of
patients undergoing early repair of Strasberg type E injuries will develop an anastomotic
stricture requiring intervention.126 Early repair with concomitant vascular injury can also lead to
increased risk of stricture given the likelihood of anastomosing a bile duct with compromised
blood ow. If a patient is unstable, septic, or has peritonitis then the repair should be delayed
because it is associated with worse outcomes.102,127 Early repair of complex injuries should only
be attempted in select cases by experienced surgeons.
Patients who are not suitable for early repair should be stabilized over the ensuing 2 to 3
months with a focus on nutrition and physical tness optimization. This convalescent period will
also allow for any porta hepatis inammation to subside and any devitalized ductal tissue to
declare itself. All intra-abdominal uid collections should be drained and active leaks should be
controlled with a combination of percutaneous catheters and endoscopic stents as discussed
above. If percutaneous catheters are draining large volumes of bile daily, then patients run the risk
of dehydration and signicant electrolyte abnormalities. In addition to meeting standard
nutritional needs, the patients electrolyte status should be monitored frequently, and the patient
should attempt to take adequate oral hydration with electrolyte rich uids to compensate for the
volume lost. Since bile is required for absorption of fat, the fat soluble vitamins A, D, E, and K may
also need oral supplementation. In rare instances bile refeeding may be required.

Techniques with immediate repair


A benet of early repair is the ease of exposure of the porta hepatis. The level of biliary injury is
often easily identied intraoperatively by either free ow of bile from the site of injury or the
presence of surgical clips at the level of injury. Any gross contamination in the abdomen should be
evacuated and the abdomen should be irrigated with sterile saline. Surgical clips are removed and
bleeding vessels are identied. The cystic artery should be sutured ligated. If a right hepatic artery
injury is suspected and thought to be repairable by an experienced surgeon, then this step should
be performed before the biliary reconstruction. However, repair of an injured right hepatic artery
is of questionable utility. Some authors argue that early reconstruction of the right hepatic artery
should be attempted to avoid potentially severe hepatic ischemia, necrosis, atrophy, or
failure.99,128,129 Injury to this vessel rarely has notable long-term sequelae and is not required
for a successful biliary reconstruction if performed in a delayed fashion by an experienced
surgeon.98,103,130 Immediate repair is not generally attempted for Strasberg E4 or E5 type injuries,
as these high injuries require signicant planning and should be temporized with wide drainage.
For Strasberg type E1-E3 injuries the transected duct should be trimmed back to healthy
tissue. The anterior surface of the common hepatic duct can be opened and extended along the
extrahepatic portion of the left hepatic duct in a fashion rst described by Hepp-Couinaud.44
This method limits devascularization of the bile duct and allows for a wide anastomosis. If this
opening is not 1.5 to 2.0 cm in length, the opening can be extended approximately 1 cm onto the
right side. Visual inspection should conrm communication between the left and right sides of
the liver before creation of an anastomosis. A hepaticoenterostomy can then be performed in a
426 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

Fig. 16. Hepp-Couinaud repair. A lateral incision is made along the extrahepatic portion of the left hepatic bile duct and a
side-to-side hepaticojejunostomy is performed using interrupted absorbable monolament suture. (Reprinted with
permission from Strasberg SM, Hawkins WG. Reconstruction of the bile duct. In: Fischer J, editor. Mastery of Surgery. 5th
ed. 2007. p. 1129-42, Lippincott Williams & Wilkins.)

side-to-side manner in the style of Hepp-Couinaud (Fig 16). Closure of the stump may facilitate
creation of the anastomosis. It is our preference to utilize a Roux-en-Y hepaticojejunostomy with
a 60 cm roux limb created in a retrocolic manner to the right of the middle colic vessels. If severe
inammation of the colonic mesentery is present, then an antecolic limb can be used.

Delayed repair techniques


Any injury resulting in the discontinuous ow of bile into the duodenum should be repaired
surgically. Most injuries requiring repair in a delayed fashion will have a biliary stent in place at
the time of operation. This is often very useful in identifying biliary anatomy in a chronically
inamed porta hepatis, especially for locating the left hepatic duct. If a PTBD was placed
preoperatively into the right ductal system it can be redirected across an intact biliary
conuence into the left hepatic duct the day before elective repair to facilitate intraoperative
identication of the left duct. Any percutaneous drain should be prepped into the operative eld
so it can be manipulated by the surgeon. Adhesions should be taken down in the porta hepatis,
gallbladder fossa, and base of the liver.
For Strasberg types E1-E3 injuries the repair begins with identication of the left hepatic
duct. This can be difcult to locate in a chronically inamed porta hepatis, but can be located
reliably by coming down the face of segment 4b along the umbilical ssure. This can be
facilitated by dividing the bridge of liver between segments 4b and 3, taking care not to injure
the left hepatic artery or bile duct at its inferior edge. If a stent is present in the left hepatic bile
duct it can be palpated to help identify the anatomy. Once the duct is identied a Hepp-
Couinaud repair can be performed.
For Strasberg type E4 or E5 injuries the left duct is identied as above, and the right duct is
identied by dropping the portal plate, dividing the brous tissue between the portal plate and
cystic plate, and carrying the incision around the lateral aspect of the porta hepatis onto
segment 1 (Fig 17).131 Care should be taken to avoid the right hepatic artery which may pass
anterior to the right hepatic duct in a contracted porta. Once adequate mobilization of the right
hepatic duct is achieved, the posterior wall of the left and right hepatic ducts can be joined with
absorbable monolament suture to aid in creating a single anastomosis in a Hepp-Couinaud
fashion (Fig 18). This technique is preferred over creating 2 separate anastomoses because the
patency rate is higher, but this may not be possible in all situations.

Operative stenting
Continued debate surrounds the routine use of bilioenteric stents following reconstruction.
Some surgeons contend that if a repair is well constructed then a stent should not be necessary.
Others will use stents selectively if the duct is small, the tissue is inamed, or if they are
otherwise worried about the viability of the anastomosis. The use of stents is not without
complication as they have been associated with pressure necrosis leading to erosion, scar
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 427

Fig. 17. Line of incision of peritoneal attachment to the liver, commencing at segment 4 and passing along the base of
segments 5, 6, and 1. Pulling the contents of the hepatoduodenal ligament to the left, and rolling the ligament in a
clockwise fashion facilitates exposure of the relevant part of segment 1. (Reprinted with permission from Strasberg and
colleagues,131 Elsevier.)

formation, or signicant bleeding via arteriobiliary stula.132,133 If a stent is decided upon, a


silastic infant feeding catheter can be used if a pre-existing stent is not in place. If a PTBD is
present, then after the anterior surface of the bile duct is incised, the tip of the stent can be
tagged with a suture, and the stent can be withdrawn into the proximal duct. This will aid in
visualization of the duct during reconstruction and the suture will allow for easy readvancement
of the PTBD back across a completed anastomosis. An additional benet of stenting with a PTBD
is the ability to easily obtain a cholangiography postoperatively to evaluate the integrity of the
anastomosis. Most patients will leave the hospital with this drain capped and have it removed at
follow-up in 2 to 4 weeks.

Fig. 18. Approximation of 2 adjacent ducts. Small, absorbable, doubled-armed, monolament is used with knots placed
on the outside of the anastomosis. (Reprinted with permission from Strasberg SM, Hawkins WG. Reconstruction of the
bile duct. In: Fischer J, editor. Mastery of Surgery. 5th ed. 2007. p. 1129-42, Lippincott Williams & Wilkins.)
428 J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435

Liver resection
For some Strasberg type E4 and E5 in which the right posterior or main hepatic duct is
injured within the parenchyma of the liver, it may be necessary to perform a limited 4B/5 liver
resection to gain enough length of bile duct and have adequate room for creating the bilioenteric
anastomosis. This partial liver resection technique may also be useful with steatotic livers where
the size of the liver limits the ability to perform the anastomosis. If the injury is so high that an
anastomosis to third order biliary radicles is required for repair, then an anatomical liver
resection may be preferable because the stricture rate with these small anastomoses is very
high. Resection may also be required in patients with severe concomitant vascular injury leading
to parenchymal death, delayed stricture, or recurrent abscesses in the injured liver. Liver
resection in this setting has had favorable results in a number of series from high volume
institutions.100,134,135

Transplantation
In very rare cases transplantation may be required in patients with severe vasculobiliary
injury.136-138 This can be required for either acute fulminant liver failure or for secondary biliary
cirrhosis due to chronic ischemia. The largest series included 20 patients with bile duct ischemia
requiring transplantation.139 In this series it took a median of 60 months from injury to receive
an organ; 4 patients died while waiting and 16 were successfully transplanted. The 5-year
survival rate was 75%, which compares favorably with graft survival results for other indications.

Follow-up
Once acute convalescence has competed, patients having undergone a biliary reconstruction
should be followed on an annual basis with a physical examination and liver function tests.
Interview questions should focus on signs and symptoms of biliary obstruction, cholangitis, or
both. It can be normal for this patient population to have persistent elevation in their liver
function tests, even after 5 years. However, elevation of alkaline phosphatase 4 166, total
bilirubin 4 1.3, alanine aminotransferase 4 62, and aspartate aminotransferase 4 66 should be
considered abnormal and prompt further investigation.140 Patients and providers should be
informed that delayed stricturing can occur up to a decade after repair.141 If delayed stricturing
does occur, nearly 90% can be resolved endoscopically.142

Long-term outcomes

Quality of life

Large database studies of outcomes in patients with bile duct injuries found that those with
an injury had a 2 to 3 times increased risk of death compared to uninjured patients. This
increased an additional 11% if the index surgeon did the repair.56 Many studies have been
performed looking at quality of life (QOL) following bile duct injury repairs; the results are
summarized in an updated table adapted from a 2016 review of this literature (Table).143-152 A
recent meta-analysis of the data available up to 2012 showed that patients were likely to have
reduced mental, but not physical QOL measures after bile duct injury.153 Improvement in QOL
measures can be slow, but may continue up to 5 years after surgical repair of biliary injuries,
with most patients returning to normal within the rst year.149

Medicolegal implications

Laparoscopic cholecystectomies are one of the most common operations to involve civil
litigation, with the most dominant adverse event.154 In a review of published jury verdicts in the
United States of 104 cholecystectomies in 48 states, 17% of cases were settled out of court, 46%
were found in favor of the claimant, and 37% were found in favor of the surgeon. If settled out of
Table
Summary of quality of life studies after bile duct injury

Studies Year Number of Control group Cases included Response rate QoL tool Duration of Reduced Reduced
of cases follow-up physical QOL mental QOL
study (mo) compared to compared to
control control

J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435


Boerma and 2001 82 ULC and general Minor and major BDI 92% SF-36 70 (37-110) Y Y
colleagues,143 population endoscopically,
Amsterdam, surgically, and
Netherlands radiologically treated
Melton and 2002 54 ULC Major BDItreated 61% Minor modication of the City 59 33 N N
colleagues,144 surgically of Hope
Baltimore, USA Medical Center Quality of
Life Survey
Moore and 2004 50 ULC Minor and major BDI 58% Karnofsky performance scale, 62 6 Y Y
colleagues,145 treated endoscopically, SF-36, psychological
Tennesse, USA surgically, and assessment to illness scale,
radiologically medical outcomes study
Sarmiento and 2004 45 ULC and general Major BDItreated 81% SF-36 100 (62-136) N N
colleagues,146 population surgically
Rochester, USA
Hogan and 2009 62 ULC Major BDItreated 78% SF-36 152 (2-240) N N
colleagues,147 endoscopically,
Dublin, Ireland surgically, and
radiologically
de Reuver and 2008 278 ULC and general BDItreated 69% SF-36, GiQLi 71 Y Y
colleagues,148 population endoscopically,
Amsterdam, surgically, and
Netherlands radiologically
Dominguez- 2014 Group 1 None, QoL Major BDItreated 33% SF-36 120 Improved Improved
Rosado and (long-term changes over surgically after repair after
colleagues,149 follow-up) time repair
Mexico 41
Group 2 90% at 1 year 12-60
(short-term 68% at 5 years
follow-up)
44

429
430
Table (continued )

Studies Year Number of Control group Cases included Response rate QoL tool Duration of Reduced Reduced
of cases follow-up physical QOL mental QOL
study (mo) compared to compared to
control control

Ejaz and 2014 62 None, QoL Major BDItreated 37% Combination of SF-36 169 Did not Improved

J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435


colleagues,150 changes over surgically GIQLI (125-222) improve after
Baltimore, USA time CLDQ after repair repair
Booij and 2017 399 ULC Minor and major BDI 63% SF-36, GiQLi 132 (84-192) Y N
colleagues,151 treated endoscopically,
Amsterdam, surgically and
Netherlands radiologically

BDI, bile duct injury; CLDQ, chronic liver disease questionnaire; GIQLI, gastrointestinal quality of life index; SF-36, short form 36; ULC, uncomplicated laparoscopic cholecystectomy; QoL,
quality of life.
J.B. Rose, W.G. Hawkins / Current Problems in Surgery 54 (2017) 406435 431

court the average award was $628,138. If the case went to trial and found in favor of the
claimant, the average award was $2.9 million.155 This trend has held up in many European
countries.152

Summary

In summary, bile duct injuries are a rare problem but can be devastating to patients when
they occur. Using a critical view of safety technique can signicantly reduce the chances of
injury. If an injury does occur, treatment should start with adequate drainage and accurate
identication of the injury. The choice of treatment modality should be thoughtful and tailored
to individual injuries. Excellent outcomes can be achieved even with severe injuries in the hands
of experienced providers.

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