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British Journal of Surgery 1995, 82, 307-313
Review
Bile duct injury and bile leakage in laparoscopic cholecystectomy
A . J . M c M A H O N , G . F U L L A R T O N * , J . N . B A X T E R T and P . J . O ' D W Y E R
University Departments of Surgery, Western Infirmary, ?Royal Infirmary, and *Department of Surgery, Gartnavel General Hospital,
Glasgow, UK
Correspondence to: Mr A . McMahon, Department of Surgery, Western General Hospital, Edinburgh EH4 2XU, UK
The introduction of laparoscopic cholecystectomy has
been associated with an increased incidence of bile duct
injury. This review presents the incidence of bile duct
injury in reported series and examines the role of the
learning curve and other contributing factors. There is
good evidence to suggest that, with adequate training and
experience, the incidence of biliary injury can be reduced
to a level comparable to that of open cholecystectomy.
Continued audit is required to ensure that the low
complication rates achieved in selected centres with wide
experience are reproduced by the surgical community in
general.
Until the end of the 1980s open cholecystectomy
remained the treatment of choice for symptomatic
cholelithiasis because of its efficacy and excellent safety
record. In the past 5 years, laparoscopic cholecystectomy
has replaced open cholecystectomy as the 'gold standard'
treatment because of the reduction in postoperative pain
and pulmonary dysfunction, shorter hospital stay and
more rapid return to normal activity'. However,
introduction of the technique has been marred by reports
of a higher incidence of major complications and, in
particular, bile duct injury2, which is a catastrophic event
that can lead to significant long-term morbidity (recurrent
stricture, cholangitis, cirrhosis and premature death)3.
This review sets out to compare the incidence of bile duct
injury after open and laparoscopic cholecystectomy, and
to establish whether the increased incidence is a problem
inherent in the newer technique, a result of the learning
curve phenomenon, or related to better reporting.
It is difficult to calculate accurately the incidence of bile
duct injury after open or laparoscopic cholecystectomy for
four reasons: first, it is an uncommon problem; second,
bile duct injury may present months after surgery; third,
voluntary audit probably results in under-reporting; and
fourth, there are variations in the definition of what
constitutes bile duct injury. Reports from specialized
centres are unlikely to represent what occurs in everyday
practice. Even surveys across the whole community, such
as that carried out by Deziel et aL4 in which surgeons
were asked to volunteer data retrospectively on biliary
complications, probably underestimate the true incidence.
Table 1 Bile duct injury rate in reported series of open
cholecystectomy
Incidence of bile duct injury after open
cholecystectomy
Table I shows that the incidence of bile duct injury in
reported
of open cholecystectomy ranges from 0
to 0.5 per cent. Thus, on average, one bile duct injury
occurs in every 200-300 cases of open cholecystectomy.
The series reported by Roslyn et ~ 1 . was
' ~ a retrospective
audit using information from computerized discharge data
from all hospitals in California and Maryland in 1989. The
91 patients (0.2 per cent) in this series with possible bile
duct injury included patients with laceration of the
Paper accepted 25 October 1994
No. of
patients
Reference
Period
Vanderpool et aL5
Ganey et al.'
Warwick and
Thompson7
Clavien et at.
Davies et al.
Saltzstein et al.
Herzog et a/.''
Morgenstern et al. l 2
Cox et a/.l 3
Roslyn et al. l4
Raute et a/.l5
Harte et al. I h
Gilliland and
Traverso17
Gouma and GoIX
Total
1976-1985
1978-1983
1982- 1990
360
1035
384
1984-1989
1985-1990
1988-1990
1984-1990
1982-1988
1985-1989
1989
1972-1991
1973- 1978
1982-1987
1088
630
500
1357
980
457
42 474
7057
390
671
1991
Bile duct
injury
8 780
66 163
~
Values in parentheses are percentages
gastrointestinal tract or biliary fistula, and the authors
therefore concluded that this was likely to be an
overestimate of the true bile duct injury rate. The highest
reported incidence was in the 1991 national survey in the
Netherlands by Gouma and Go1s, in which there were 45
injuries in 8780 open cholecystectomies, of which 18 (0.2
per cent) required hepaticojejunostomy. Five patients
needed end-to-end anastomosis, three strictures required
endoscopic stent insertion and 15 injuries were closed
primarily without T tube drainage (in four the treatment
was not specified). Four of the 45 patients died as a
consequence of the bile duct injury. In the report by
Raute et al. of 16 (0.2 per cent) bile duct injuries in 7057
open cholecystectomies performed over a 20-year period,
only three (0.04 per cent) required hepaticojejunostomy;
the management in the others consisted of end-to-end
anastomosis in three, T tube insertion in eight, endoscopic
stricture dilatation in one and percutaneous or nasobiliary
drainage in one. One patient initially treated by T tube
drainage subsequently required hepaticojejunostomy. The
final outcome of repair was good in all but one patient
307
308 A . J . M c M A H O N , G . F U L L A R T O N , J . N . B A X T E R and P . J . O ' D W Y E R
with hepaticojejunostomy who had occasional episodes of
cholangitis. Only one of the eight other bile duct injuries
reported in the series shown in Table I required biliary
reconstruction; the remaining seven were managed by T
tube insertion (two patients), peritoneal drainage (three),
suture of the laceration (one) and stricture dilatation
(one).
Incidence of laparoscopic bile duct injury
Several early report^'^,^^, some of which were anecd ~ t a l ~ l suggested
-~~,
that laparoscopic cholecystectomy
was associated with an increased bile duct injury rate
compared with open cholecystectomy. In a series of 400
operations Troidl et aLZ0reported four (1.0 per cent) bile
duct injuries, one of which resulted in death. TraversoZ3
reported 17 (2.8 per cent) common bile duct (CBD)
injuries in a series of 597 operations. In 264 laparoscopic
cholecystectomies performed in ten hospitals in the southeast of England, there were five (1.9 per cent) bile duct
injuries, four of which required hepaticojejunostomyZ2.
Smith2] interviewed biliary surgeons attending the
American College of Surgeons meeting in 1991. All
surgeons reported that bile duct injuries from
laparoscopic cholecystectomy were occurring out of all
proportion to those encountered at open cholecystectomy.
From the first four surgeons interviewed Smith 'gleaned'
more than 30 bile duct injuries. He went on to comment
that for the non-specialist occasional cholecystectomist
'laparoscopic cholecystectomy was a recipe for disaster a keyhole scar and catastrophe within'. These increased
risks have received coverage in the national press25.
Perhaps the most important indicator is that specialist
hepatobiliary units on both sides of the Atlantic have
noted a dramatic increase in the number of referrals for
management of bile duct injury2,22,26-30.
Most single-centre series of more than 300 laparoscopic
cholecystectomies have described a bile duct injury rate of
less than 0.4 per cent, with an overall mean of 0.3 per
cent15,31-47, although three series20.4s.49reported an
incidence of 1 per cent or more (Table 2 ) . By contrast, 12
of 21 multicentre audit series described a bile duct injury
rate greater than 0-4 per cent, with an overall mean of 0.5
per cent4.s0-66 (Table 3 ) . Two factors may explain this
discrepancy. First, it is well recognized that bias occurs in
the publication of a new procedure; serious complications
and poor results are less likely to be mentioned67.Second,
the single-centre series are gathered by surgeons who
have performed large numbers of procedures and who are
therefore far up the 'learning curve'; the majority of
surgeons in audit series are probably lower on the curve.
Taking both factors into account, an estimate across the
surgical community as a whole of one bile duct injury in
every 100-200 cases of laparoscopic cholecystectomy
seems reasonable.
Classification of bile duct injury
Type of injury may be subdivided into bile duct laceration,
bile duct transection or excision, and bile duct stricture.
The level of stricture may be further graded according to
Bismuth's classification6*(Table 4 ) . The rognosis of a bile
duct injury depends on the nature of t e lesion. A small
longitudinal tear, which is immediately repaired by
primary suture or insertion of a T tube, has a quite
different prognosis from completed division of the bile
R
Table 2 Bile duct injury in reported series of laparoscopic
cholecystectornycontaining more than 300 patients from single
centres
No. of
patients
Reference
KO and Airan3I
Nottle32
Fitzgibbons et al.33
Wilson et ~ 1 . ' ~
Wolfe et al."
Taniguchi et
Lane and
Lanthro~~~
Baird et al.3x
Graffi~~~
Raute et a1.I5
Barkun et al.4o
Soper et ~ 1 . ~
Clair et aL4Z
Brown et aL4'
Berci and
Sa~kier~~
Davis et al.45
Graves et al.46
Perissat et at.47
Troidl et aLZ"
Huang et al. 4x
Kozarek et aL4'
Total
Bile duct
injury
300
308
350
350
381
600
641
800
900
1022
1300
647
514
474
418
~
622
304
700
400
350
597
11978
Values in parentheses are percentages
Table 3 Bile duct injury in multicentre audit series of
laparoscopic cholecystectomy
~
~
~
No. of
patients
Bile duct
injury
Reference
Place
Litwin et aLSu
Airan et aLS1
Cocks et al.sz
Larson et aLs3
Devenys4
Dunn et al. ys
Orlando et ~ 1 .
Cuschieri et aLS7
McGee et aLSx
Macintyre and
Wilsonss*
Southern Surgeons
Club'"
Deziel et aL4
Gigot in
Suc et al.6"
Kimura eta[."
Trondsen et al. 62
Collet et al.63
Suc et at."
Fullarton et aLM
Go et aL6'
Macintyre and
Wilsonss*
Kum and Goh66
Canada
USA
Australia
USA
Oregon, USA
England
~ ~
Connecticut,
USA
Europe
USA
Switzerland
2201
2671
6 000
1983
9 597
3319
4 640
1236
950
1091
3 (0.1)
5 (0.2)
12 (0.2)
5 (0.3)
27 (0.3)
11 (0.3)
15 (0.3)
4 (0.3)
3 (0.3)
5 (0.5)
USA
1518
7 (0.5)
77 604
3 244
365 (0.5)
16 ( 0 5 )
1989
527
2 955
3 606
1655
6 076
2 888
11 (0.6)
3 (0.6)
18 (0.6)
25 (0.7)
11 (0.7)
52 (0.9)
26 (0.9)
Total
USA
Belgium
Japan
Norway
France
France
Scotland
Netherlands
Japan
Singapore
1066
10 (0.9)
136816
634 (0.5)
Values in parentheses are percentages. *Presented at the 3rd
World Congress of Endoscopic Surgery, Bordeaux, France in
1992
British Journal of Surgery 1995, 82, 307-313
BILE DUCT INJURY IN LAPAROSCOPIC CHOLECYSTECTOMY
Table 4 Bismuth classification”xof bile duct strictures
Grade
Description
0
1
2
3
4
5
Common bile duct
Low stricture ( > 2 cm CHD)
Middle stricture ( < 2 cm CHD)
High stricture (confluence preserved)
High stricture (confluence destroyed)
Right anomalous duct
CHD, common hepatic duct
Table 5 Proposed definition of major and minor bile duct injury
Major bile duct injury (at least one of the following present)
Laceration > 25 per cent of bile duct diameter
Transection of common hepatic duct or CBD
Development of postoperative bile duct stricture
Minor bile duct injury
Laceration of CBD < 25 per cent of diameter
Laceration of cystic-CBD junction (‘buttonhole’tear)
CBD. common bile duct
ducts above the bifurcation, which goes unrecognized and
is repaired after a delayed interval. Therefore, a
subdivision into major and minor ductal injury is proposed
in Table 5. Minor injury can usually be managed by simple
suture repair and/or insertion of a T
Major injury
usually requires h e p a t i c o j e j u n o ~ t o m y ~ ~ ~ ~ * ~ ~ ~ ~ ~ .
309
Laparoscopic bile duct injury tends to be more severe
than that which occurs during open cholecyste~tomy~~.
A
portion of the duct is typically resected, the proximal level
of the injury is high (Bismuth type 3 or 4) and the duct
diameter is usually small, all of which make for a poorer
prognosis after repair73.
Causes of laparoscopic bile duct injury
There are several reasons why the bile duct may be more
vulnerable during laparoscopic cholecystectomy and the
anatomy misidentified. The camera provides a monocular
view from a direction quite different from that of open
surgery; the CBD is not usually seen from this angle.
Cephalad traction on the fundus compresses Calot’s
triangle, while lateral traction on Hartmann’s pouch tents
up the CBD, which may then be mistaken for the cystic
duct, especially when that duct is very short. Another
cause of greater risk is the use of diathermy around
Calot’s triangle74; this is rarely used during open
cholecystectomy.
In the early days of laparoscopic cholecystectomy, laser
technique was popular, particularly in the USA. There is
anecdotal evidence that this is more dangerous than
diathermy dissection since the laser beam may be applied
inadvertently to the bile duct or past-pointing of the laser
beam may O C C U ~ ~ It* ~has
~ . subsequently been shown that
laser therapy offers no benefit over diathermy
dis~ection~~
Its. use should certainly be avoided
completely in Calot’s triangle.
The laparoscopic ‘learning curve’
There is substantial evidence to suggest that the learning
Types of laparoscopic bile duct injury
curve has contributed to the high rates of bile duct injury.
Several types of laparoscopic injury occur2,22*26-30,48,69,70. In the Southern Surgeons Club series59, the bile duct
The classical one involves misidentification of the
injury rate in the first 13 patients operated on by each
common duct for the cystic duct: the common duct is
clipped and divided, the common hepatic duct is resected
and the proximal biliary tree clipped and divided (the
right hepatic artery is usually also injured because of its
proximity). A variant of the classical injury is seen when
the CBD is clipped and divided distally and the cystic duct
is correctly clipped and divided, leaving a complete biliary
fistula. Another common injury occurs when tenting
results in a portion of the common duct being removed
between clips. This may cause stricture, complete
obstruction or a fistula. A third injury occurs when the
right hepatic duct is misidentified as the cystic duct, and
clipped and divided.
There is a suggestion that bile duct injury that occurs
during laparoscopic surgery is less likely to be detected at
the time of operation than that occurring during open
cholecystectomy. In the study of Gouma and GoI8 55 per
cent of injuries during open cholecystectomy were noted
at the time, compared with 34 per cent during
laparoscopic cholecystectomy. This has implications for
prognosis, as delay in recognition reduces the chance of
successful repair.
Strictures may present weeks or months after
laparoscopic cholecystectomy2. Most are thought to be
due to injudicious use of diathermyz7,but some may result
from partial obstruction by misplaced clips71. Duct
laceration may be caused by diathermy or scissor injury.
In most series the bile duct injuries have not been
associated with aberrant anatomy26,29,48,72.
British Journal of Surgey 1995, 82,307-313
surgical group was 2.2 per cent, compared with 0.1 per
cent for subsequent patients. In the national survey of
hospitals in the USA4, the average bile duct injury rate
was 0.65 per cent in institutions that had performed fewer
than 100 laparoscopic cholecystectomies, compared with
0.42 per cent at hospitals with more than 100 performed.
Similarly, in the Connecticut state audits6, eight of the 15
bile duct injuries occurred during a surgeon’s first ten
cases, five between cases 11-50 and only two after case
50. Of 17 biliary injuries or leaks reported by Kozarek et
u Z . ~ ~ 13
, occurred within the first 20 procedures performed
by the surgeon. In Davidoff and colleagues’ report of 12
bile duct injuries, ten occurred within the first 11
laparoscopic proceduresz7. Further evidence that the
increased incidence of laparoscopic bile duct injury is
related to the learning curve is contained in a report of 81
injuries from three tertiary referral centres70. The number
of referrals peaked during 1991, and in 1993 declined to
an incidence typical of the prelaparoscopic era. Data on
open cholecystectomy are also worthy of note: in a report
of 65 bile duct injuries, 55 (85 per cent) were inflicted by
unsupervised surgeons in training77.
The European Association of Endoscopic Surgeons has
recently published guidelines on the minimum acceptable
level of training before a surgeon be allowed to perform
laparoscopic cholecystectomy unsupervi~ed~~.
Among the
conditions are attendance at a recognized endoscopic
course, supervision during the first five procedures and
written review of the results of the first ten operations.
3 1 0 A . J . M c M A H O N , G. F U L L A R T O N , J . N. B A X T E R and P. J . O ’ D W Y E R
Role of cholangiography
The development of laparoscopic cholecystectomy has
rekindled a long-standing and unresolved debate about
the value of routine cholangiography. Severa12s.48~79,so
authors have suggested that the routine use of operative
cholangiography might prevent bile duct injury. It is
argued that it may help in further defining anatomy
(particularly if it is aberrant) and, in the event of a bile
duct already being injured, allow early recognition and
immediate repair. Other a ~ t h o r s ~ ~have
, ~ ~ contested
,~’
this view. In a review of published series of laparoscopic
cholecystectomy, Macintyre et al. 55 found no correlation
between the incidence of bile duct injury and the
frequency of operative cholangiography. Barkun and cow o r k e r ~ performed
~~
a series of 1300 laparoscopic
cholecystectomies, using operative cholangiography
selectively in only 54 (4.2 per cent). Five bile duct injuries
occurred (0.4 per cent), but the authors concluded that in
only one of the cases would routine cholangiography have
led to earlier recognition of duct injury. Andren-Sandberg
et ~ 1described
. ~ ~a series of 65 bile duct injuries occurring
during open cholecystectomy, with operative cholangiography performed in 62 (95 per cent) of the cases: the bile
duct was injured before cholangiography in 44 per cent of
cases and after normal cholangiography in 53 per cent.
Several
who do not perform routine
cholangiography have reported large series of
laparoscopic cholecystectomies without major bile duct
injury. Most surgeons in the UK (85 per cent) do not
perform routine cholangiographys4 and some bile duct
injuries are known to result from the cholangiography
catheterIs. A large randomized trial has concluded that
operative cholangiography need be performed during
cholecystectomy only when clinical criteria suggest the
presence of CBD abnormalities or when there is a need to
clarify ductal anatomy8s,86.
Avoiding laparoscopic bile duct injury
Steps to avoid laparoscopic bile duct injury have been
advocated by several a ~ t h o r s ~ ~ - * ~ ~ ~ ~ ~ ~ ~ ) .
1 Ensure an optimal view of the operating field.
2 Always dissect away from the gallbladder.
3 Minimum use should be made of electrocoagulation in
Calot’s triangle (laser should be avoided completely in
this area).
4 The anatomy of Calot’s triangle should be completely
clear before the cystic duct and artery are clipped or
divided. The junction between gallbladder neck and
cystic duct should be clearly demonstrated.
5 The procedure should be converted early to open
cholecystectomy if the anatomy cannot be safely
identified or troublesome bleeding occurs.
A number of different techniques are used to perform
laparoscopic cholecystectomy (hook dissection versus
blunt or scissors dissection, diathermy versus laser) with
apparently equal success. A number of additional
technical points have been suggested by several authors to
help avoid laparoscopic bile duct injury, but are not used
by all surgeons.
1 Use a 30” telescope that allows different angles of
view, gives an en face view of Calot’s triangle, and
often allows visualization of the CBD.
Obtain maximum cephalic traction on the fundus of
the gallbladder, which brings Calot’s triangle into view
and reduces redundancy of Hartmann’s pouch.
Retract laterally on Hartmann’s pouch, which opens
out Calot’s triangle and creates a sharper angle
between cystic duct and CBD.
Dissect along the posterolateral aspect of the
gallbladder to free the neck of the gallbladder from
the liver bed.
Keep dissection of the gallbladder close to its wall.
As in open cholecystectomy, retrograde dissection is a
useful technique if there is severe inflammation.
Perform operative cholangiography if there is any
doubt about the anatomy.
Bile leak
Bile leak after cholecystectomy may result in an intraabdominal collection, biliary fistula or biliary peritonitis,
which is a life-threatening complication. It may arise from
three sources: the cystic duct, a subvesical bile duct (duct
of L ~ s c h k a ~or
~ , a~ bile
~ ) duct injury (the last usually
being considered separately in the classification of
complications). The subvesical duct of Luschka is a
slender duct, 1-2 mm in diameter, which passes from the
right lobe of the liver in the gallbladder fossa to join the
right hepatic or common hepatic
Because of its
position and small size, it is particularly vulnerable during
cholecyste~tomy~~.
Anatomical studies, using resin casting,
dye injection and histology of cadaver livers, have shown
that a subvesical duct is present in about 30-50 per cent
of patients, although endoscopic retrograde or operative
cholangiography detects it in only 1.3 per cent”.
The reported incidence of bile leakage after open
cholecystectomy varies considerably. In several recent
large audit series of open cholecystectomy, there were no
bile
Clavien et aLs reported four (0.3
per cent) leaks requiring reoperation in a series of 1252
open cholecystectomies. Morgenstern and co-workers’*
reported six (0.5 per cent) leaks resulting in fistula in a
series of 1200 cholecystectomies; all six resolved
spontaneously. In a series of 196 cholecystectomies in
which routine drainage of the gallbladder bed was used
for an average postoperative duration of 6days, bile was
noted in the drain fluid in 19 (9.7 per cent), but only one
patient (0.5 per cent) required a second procedures7. The
source of bile leakage after open cholecystectomy is often
not positively identified but cystic duct leakage is thought
to be extremely rare.
Bile leakage occurs with greater frequency after
laparoscopic cholecystectomy2n~42~49~61~6s~92
Wolfe et al. 3s
reported five (1.3 per cent) clinically significant
postoperative leaks in a series of 381 laparoscopic
cholecystectomies; four were from the cystic duct, of
which three required operation. Peck24reported nine (1.9
per cent) leaks in a series of 482 laparoscopic
cholecystectomies, six of which were from the gallbladder
bed. Walker et ~ 7 1 described
. ~ ~
seven (2.7 per cent) bile
leaks in a series of 264 procedures. Trondsen et aL6’
reported ten (1.9 per cent) bile leaks in a series of 527
laparoscopic cholecystectomies; four were from the cystic
duct stump (all requiring laparotomy) and six from
subvesical bile ducts (one requiring laparotomy).
There are a number of reasons why laparoscopic
cholecystectomy may be associated with a greater risk of a
bile leakage. Clips rather than ties are used for the cystic
British Journal of Surgery 1995, 82, 307-313
B I L E D U C T I N J U R Y IN L A P A R O S C O P I C C H O L E C Y S T E C T O M Y
duct. Cystic duct leakage may occur if a clip becomes
dislodged”, if a clip does not completely traverse the duct
or if electrocautery injury results in delayed tissue necrosis
of the cystic
Leakage from injury to the cystic
duct distal to securing clips has also been described”.
During laparoscopic cholecystectomy the gallbladder is
usually dissected from the liver bed with diathermy,
whereas at open cholecystectomy this is usually done by
blunt or sharp dissection. It is possible that the subvesical
duct is at greater risk of accidental damage during
laparoscopic cholecystectomy because of the depth of
thermal injury caused by electrocautery dissection.
Conclusion
Laparoscopic cholecystectomy has been introduced into
routine surgical practice with unprecedented speed. Its
introduction has been marred by reports of a higher
incidence of bile duct injury. While there is evidence to
suggest that the incidence of bile duct injury is falling as
surgeons gain greater experience with the laparoscopic
technique, careful audit is required to establish the true
risk of injury. Avoidance of bile duct injury may require
more closely regulated supervision of trainee
laparoscopists. The use of safe techniques for defining
biliary anatomy and early conversion to open operation
when the anatomy is unclear may also reduce the risk of
duct injury.
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10
II
12
13
McMahon AJ, Russell IT, Baxter JN et ul. Laparoscopic
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