DOI: 10.1002/jhbp.

710

SYST E M AT I C R E V I E W

Minimally invasive surgery for the management of major bile

duct injury due to cholecystectomy

Francesco Guerra   | Diego Coletta   | Manuel Gavioli  | Danilo Coco  | Alberto Patriti

Division of General Surgery, Ospedali

Riuniti Marche Nord, Pesaro, Italy
Correspondence
Francesco Guerra, Division of General
Surgery, Ospedali Riuniti Marche Nord,
Piazzale Cinelli 3, 61100 Pesaro, Italy.
Email: fra.guerra.mail@gmail.com
Abstract
Background: In recent years there has been a growing interest in the application of
minimally invasive surgery in the management of cholecystectomy-related injury to
the biliary tract. The aim of this analysis was to identify and combine the available
evidence on the argument, with particular reference to major injuries to the main bile
duct requiring biliodigestive anastomosis.
Methods: The PubMed/MEDLINE, Embase, and Web of Science electronic data-
bases were queried through May 2019. Inclusion criteria considered all studies re-
porting detailed data about patients with bile duct injury following cholecystectomy
receiving minimally invasive (both laparoscopic and robotic) surgical repair. Clinical
outcomes data were pooled and analyzed.
Results: A total of 31 studies reporting on the outcomes of 218 patients were eventu-
ally included in the analysis, whereby 148 patients with type D or E injury. Of these,
there were 31 patients (21%) receiving direct bile duct repair and 117 patients (79%)
undergoing bilioenteric reconstruction. Among patients with major bile duct injury,
postoperative morbidity was 24%, being 12% the incidence of major complications
and 6% the rate of patients requiring subsequent, further surgery.
Conclusions: The absence of high-level evidences precludes the possibility to draw
definitive conclusions. However, the available data derived from a growing number
of centers demonstrate that minimally invasive surgery may offer its well-known
advantages on postoperative outcomes also in the setting of severe iatrogenic injury
to the bile ducts.

KEYWORDS
bile duct injury, hepaticojejunostomy, laparoscopic cholecystectomy, minimally invasive surgery

1  |   IN T RO D U C T ION are generally responsible for significant patient disability and

Although in recent years the incidence of bile duct injury
(BDI) sustained during laparoscopic cholecystectomy (LC)
has decreased to rates comparable to the open era,1,2 it is still
one of the most serious iatrogenic surgical complications,
with an impact on patients' quality of life and health care
costs that can be devastating.2‒5 Actually, biliary tract lesions
long-term sequelae represent a major source of litigation in
most countries.6‒9
The intraoperative recognition of BDI following LC has
been traditionally regarded as a relative indication to convert
the procedure into an open repair.5,9‒11 Similarly, when the
diagnosis is made postoperatively, surgery is ordinarily un-
dertaken by the conventional open approach, especially if

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158      GUERRA et al.

a major injury to main bile ducts is suspected.5,12‒15 This is grades I and II, while major complications as grade III–IV
essentially due to the need to perform meticulous reconstruc- events. All accessible data were retrieved from each included
tion often requiring bilioenteric anastomosis. The main lim- study according to an intention-to-treat principle  of analysis.
itations to the recurse to minimally invasive techniques are When multiple reports by the same groups did provide dupli-
in relation to the technical difficulties posed by the presence cate data with overlap among patients, the most detailed or the
of severe adhesions, septic collections, and the difficulty to most recent data were considered.
recognize relevant anatomy.6,9,10 The PRISMA (Preferred Reporting Items for Systematic
Despite this, in recent years the application of minimally reviews and Meta-Analyses)19 checklist was used to perform
invasive surgery (MIS) has been reported by several leading the review, while the Cochrane handbook for systematic re-
centers with promising results suggesting possible advan- views of interventions guidelines was used to evaluate the
tages over conventional surgery.9‒11 Nevertheless, it is still methodological quality of the included studies.20
difficult to define the actual impact of MIS in treating chole- This review involved solely already published clinical re-
cystectomy-related BDIs, as most of the available data are de- search, and therefore, no IRB approval was sought.
rived from anecdotal reports or single-institution case series,
which are generally flawed by low caseload and significant
selection bias.1,11 3  |  RESULTS
Accordingly, the purpose of this analysis was to system-
atically review the scientific literature to aggregate the avail- Our initial search yielded 1373 records. After the exclusion of
able evidence on the application of MIS to the management duplicate records, titles and abstracts were appraised. Full texts
of injury to the biliary tract sustained in the course of cho- were thus evaluated, including the relative references of each
lecystectomy, with particular reference to the injuries to the study. Finally, a total of 31 reports were included in the analy-
common hepatic/main bile duct. sis.1,9‒11,21‒47 The PRISMA diagram is given in Figure 1.
In all studies, clinical heterogeneity was noticeable
mostly because of the lack of detailed endpoints. In gen-
2  | METHODS eral, specific detection and selection biases were present
in all of the included studies, basically in relation to the
Two authors (DC, FG) queried the PubMed, Embase and absence of detailed diagnostic criteria, the lack of system-
Web of Science electronic databases independently up to atic and reproducible postoperative assessment and, impor-
May 2019.16 A combination of the following search strings tantly, the non-univocal diagnostic criteria used to define
was used: “iatrogenic bile duct injury” or “relaparoscopy” or the mechanism of BDI.
“bile leak” and “laparoscopic cholecystectomy”. The included studies were published between 1990 and
Our search strategy was restricted to English language. 2019. A total of 218 patients of median age ranging be-
The authors appraised the titles and abstracts of the retrieved tween five and 84 years were included in the final analysis.
records. The full text of each potentially eligible study was
appraised and relative references were thus searched to find
further citations suitable for inclusion.
All published clinical studies that included minimally inva-
sive surgical treatment (both laparoscopic or robot-assisted) of
patients with cholecystectomy-related injury to the main bile
duct were considered for further analysis. Studies that did not
provide specific details on surgical procedures and/or postoper-
ative outcomes were excluded. Studies reporting on endoscopic
treatments adjuvated by laparoscopic peritoneal lavage were
also excluded. Where available, BDIs were reported according
to the Bismuth-Strasberg classification.17 Details concerning
the postoperative course were searched to analyze the relative
incidence of surgical and medical morbidity, the length of hos-
pital stay following surgery, and the percentage of patients re-
quiring reoperation. Available data about long-term outcomes
were also assessed with regard to the incidence of late anasto-
motic complications. Postoperative morbidity was graded ac-
cording to the classification of surgical complications proposed
by Clavien et al.18 so that minor complications are defined as F I G U R E 1   The flow diagram illustrating the selection process
GUERRA et al.
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Based on the information provided by each study, there
were 70 patients (32%) with types A to C injury, and 148
patients (68%) with injury to the common hepatic/main
bile duct (type D or E). Table 1 summarizes the charac-
teristics of the included studies reporting on patients with
type D or E BDI, with relative patients baseline character-
istics and main outcomes. The interval between cholecys-
tectomy and definitive repair differed significantly among
studies, ranging from immediate treatment (intraoperative
diagnosis and direct repair) to 8 years. Overall, postopera-
tive morbidity was 20%, while the incidence of major com-
plications was 10% (specific data derived from 17 studies
including 169 patients).
Globally, there were 148 patients with type D or E BDI
who received MIS repair, whereby 84 by conventional lap-
aroscopy and 64 by robotic laparoscopy. Injuries included
varied from type D to E5 according to Strasberg et al.
Thorough analysis of the data provided by each included
study revealed there were 23 patients with type D and 116
patients with type E injury, whereas a definitive classifica-
tion was not possible for nine patients. Surgeries consisted
of either direct repair of the main bile duct, either recon-
struction by means of biliodigestive anastomosis. Overall,
postoperative morbidity was 24% (34 out 141 patients with
accessible data), being 12% the relative incidence of major
morbidity (17 out of 141 patients), including a total of 6%
of patients (eight out of 141 patients) requiring redo-sur-
gery. The median length of postoperative hospital stay was
7  days, and ranged between 2 and 19  days (data from 14
studies including 136 patients). No surgery-related mortal-
ity occurred.
Of 31 patients (21%) received direct repair of the biliary
tract. Of these, nine patients received direct suture,33,35,41,44,46
while the remaining 18 patients underwent bile duct su-
ture (either partial suture or end-to-end anastomosis) over
T-tube.29,30,33,34,38,41,44 7% of procedures were converted
into an open surgery (two out of 27 patients with operative
details). Postoperative morbidity for this specific group of
patients receiving direct repair to the biliary tree was 20%
(four out of 20 patients with detailed data from three stud-
ies). Details about long-term follow-up were not available.
A total of 117 patients with BDI treated by minimally
invasive surgical repair featuring a biliodigestive anasto-
mosis were identified (79%). Of these, 53 patients (45%)
underwent conventional laparoscopic surgery, while 64 pa-
tients (55%) received surgery with the robot. As for surgical
procedures, 109 patients (94%) were treated with standard
Roux-en-Y hepaticojejunostomy (HJ),1,9‒11,25,26,36,37,42

T A B L E 1   General characteristics and main findings of included studies

Study Patients Type of injury Time to redo Repair Overall morbidity LOS (d)
1
Ayloo et al 1 E (E1) 7 d R-HJ 0% 3
Chen et al25 3 – 2–56 d L-HJ 66% 6.4 ± 2.0
26
Chowbey et al 4 E (E1–E2) 1–3 wk L-HJ 25% 4a
Cuendis-Velázquez 75 E (E1–E5) 20 d (7–80) L-HJ/R-HJ 25.3% 7 (5–10)
et al11
Dokmak et al10 3 – 45–300 d L-HJ 0% 7–9
29
Farinetti et al 1 E (E1) 21 d Direct repair 100% –
Fu et al30 1 D 2 d Direct repair – –
9
Giulianotti et al 14 E (E1–E5) 45.9 ± 23.4 d R-HJ 29% 8.4 ± 6.7
Kwak et al33 13 D, E (E1–E5) 0–2 d Direct repair 12.5%a 4.5 (3–21)a
Lien et al34 1 D 0 Direct repair 0% –
35
Machado et al 1 E3 >6 wk Direct repair 0% 4
Machado et al36 1 E3 8 y R-HJ 0% 4
37
Marino et al 12 E (E1–E4) 7 d (3–11) R-HJ 16.7% 9.4 (6–13)
Martin et al38 2 D 0–6 wk Direct repair 50% –
40
Palermo et al 1 E (E1) – L-HJ 0% 3
41
Pekolj et al 4 D – Direct repair 60% –
Prasad et al42 1 E (E2) 2 mo R-HJ 0% 4
44
Tantia et al 9 D 0 Direct repair/L-CJ 0% 4 (2–5)
Wills et al46 1 D – Direct repair – 4a
Time to redo and LOS are reported as direct values, ranges, medians (with ranges) or means ± standard deviations, as provided by each included study.
Abbreviations: L-CJ, laparoscopic choledochojejunostomy; L-HJ, laparoscopic hepaticojejunostomy; LOS, length of hospital stay; R-HJ, robotic hepaticojejunostomy.
a
Indirect data.
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160      GUERRA et al.
while eight patients received alternative procedures includ-
ing Roux-en-Y choledochojejunostomy,44 left hemihepa-
tectomy and HJ,36 Roux-en-Y bi-HJ,9 the Kasai procedure,9
redo-HJ,40 and HJ on a previous Roux-en-Y gastric by-
pass.9 The overall rate of conversion to an open procedure
was <1%, ranging from 0 to 25% among studies. Twenty-
eight patients experienced complications during the post-
operative course, defining an overall morbidity of 24%. In
particular, the relative rate of major morbidity was 11% (13
patients).
Seven studies (including a total of 110 patients) provided
detailed data about postoperative follow-up, which ranged
between 6  months and >4  years. Among these, there were
seven cases of clinically relevant anastomotic stricture (rel-
ative incidence 0.9%), of which four patients were success-
fully managed by endoscopic dilation, whereas three required
re-intervention by conventional open (one patient) or robotic
surgery.
4  |   D IS C U SS ION
The last 20 years have seen a growing application of mini-
mally invasive techniques for surgery of the liver and bil-
iary tract, mainly because of the growing experience of
many surgical teams and availability of innovative tech-
nologies.9,11,48,49 Still, the surgical repair of iatrogenic
BDIs has been historically considered a demanding pro-
cedure for which the implementation of MIS has been
more cautious to proceed.6,11,15,49 This is due to a number
of factors. First, almost invariably surgical anatomy is ob-
scured by the presence of intra-abdominal collections, ad-
hesions and a highly variable number of surgical clips and/
or ties. Secondly, while a minimally invasive management
of minor bile leaks is generally feasible, the need to fash-
ion a bilioenteric anastomosis may pose several technical
difficulties when the procedure is to be performed laparo-
scopically. In addition, the evident paucity of reports of
entirely minimally invasive bilioenteric anastomosis does
not encourage surgeons to recourse to MIS in the setting of
iatrogenic injury.
Despite this, the application of MIS in the management of
cholecystectomy-related BDI has increased over recent years,
with a number of experienced centers worldwide reporting
promising results.9,11,25,26,37 However, general conclusions
are difficult to draw, as the currently available data are mainly
derived from studies of low-level evidence reporting highly
variable outcomes.1,9,11,25,26,35‒37 Accordingly, the aim of our
study was to pool the available evidence from the literature
to define the actual role of MIS in the surgical repair of BDI
due to cholecystectomy.
Globally, this comprehensive, systematic review pro-
vides on a large scale the evidence-based confirmation of the
feasibility and effectiveness of the minimally invasive-option
for repair of post-cholecystectomy BDI. It is the first analysis
to combine and summarize the existing evidence upon the
argument, providing the general outcomes of patients with
BDI treated by MIS and specifically the relative outcomes
of patients with BDI receiving definitive repair by means of
minimally invasive biliodigestive reconstruction. The data
provided are crucial to compare the outcomes of a grow-
ing number of patients being treated minimally invasively
with those of patients receiving surgery with conventional
approaches.
The overall rate of type D or E BDI patients with post-
operative complications was 23% in the present analysis. Of
note, the specific incidence for patients receiving minimally
invasive bilioenteric anastomosis was 24%. Overall, these
data compare favorably with that reported following open re-
pair with HJ by experienced surgical teams.12,14,15,50,51 One
of the first, consistent data reports on the surgical manage-
ment of major cholecystectomy-related BDI was published by
Sicklick et al. in 2005.12 In their series, the authors pooled the
perioperative outcomes of 172 hepaticojejunostomy and three
end-to-end repairs performed over a 13-year period. Overall,
postoperative morbidity was 43%. Notably, wound infection
(8%), cholangitis (6%), and intra-abdominal abscess (3%) were
the most frequent surgical complications. Nonsurgical postop-
erative complications included cardiopulmonary (7.4%), infec-
tions (6.9%), and minor gastrointestinal (5.1%) complications.
Postoperatively, cholangiography revealed an anastomotic leak
in less than 5% of patients. The median length of postopera-
tive hospitalization was 9 days (1–57). Overall, the timing of
definitive BDI repair did not impact on the incidence of post-
operative complications.12 More recently, Dominguez-Rosado
et al retrospectively reviewed their Institutional database in-
cluding a large number of patients (>600) who underwent sur-
gical repair of cholecystectomy-related severe (E1–E4) BDI
by HJ.50 The authors found that 30% of patients had compli-
cations, with wound infection and postoperative pneumonia
being the most frequent (16 and 5%, respectively). Overall,
anastomotic failure (clinically relevant stricture or recalci-
trant cholangitis requiring re-intervention) occurred in more
than 20% of patients. In this regard, the extremely low rate
of anastomotic failure requiring intervention (surgical, endo-
scopic or both) identified by our review should be interpreted
with caution. Most strictures develop after more than 1 year
following surgery4 and the follow-up information from most
of the primary studies are insufficient to provide reliable data.
With direct regard to major postoperative complications, the
aggregated data of patients receiving bilioenteric anastomosis
for major BDI revealed a rate of 11% in our review. These data
are interesting as compared to the proportion of patients expe-
riencing major morbidity following conventional open HJ.13,15
The European-African Hepato-Pancreato-Biliary Association
recently reported on an impressive number of consecutive
GUERRA et al.
patients (>900 patients from 48 centers) who received HJ
following BDI.13 Overall, major morbidity (defined as grade
III-IV according to Clavien et al18 ranged between 15 and 22%.
One aspect of our analysis merits further consideration.
The present review aggregates the outcomes of patients re-
ceiving minimally invasive BDI repair along a period greater
than 25 years. Interestingly, in the case of biliodigestive re-
construction the application of conventional laparoscopy
accounts for less than half of procedures, while most surger-
ies have been undertaken with the robot only during the last
5 years.9,11,37 This reflects precisely the recent evolution of
clinical practice in the setting of complex liver and pancreatic
surgery, for which the robot is offering a valid option to facili-
tate and widen the range of applications of MIS, as compared
with standard laparoscopy.48,49
In this regard, Cuendis-Velazquez et al recently published
a retrospective comparative analysis on patients with iatro-
genic BDI receiving conventional laparoscopic versus ro-
botic standard HJ over a 7-year period. In total, 75 patients
with E1–E5 BDI were included in the analysis. Overall, the
robot resulted in slightly superior outcomes as compared to
conventional laparoscopy, in terms of both overall postop-
erative morbidity and anastomotic patency, though without
statistical significance. Giulianotti et al from the University
of Chicago9 recently reported a series of consecutive robotic
procedures for the management of iatrogenic bile duct inju-
ries following laparoscopic cholecystectomy. The authors ag-
gregated the results of 14 procedures performed over a 9-year
period. A single Roux-en-Y HJ was performed for recon-
struction in most cases. Interestingly, the robot allowed for
highly demanding procedures such as Roux-en-Y bi-HJ, and
HJ fashioning on a previous Roux-en-Y gastric bypass. The
results were encouraging, despite the presence of these very
complex cases within the series. Among the merits of a min-
imally invasive treatment, the authors suggested also possible
advantages in relation to medico-legal aspects.9
Several limitations to the present analysis must be ac-
knowledged. Firstly, the low methodological level of most
of the included studies, essentially in relation with the like-
lihood of several reporting biases, may have affected the
general results. In particular, diagnostic criteria for postop-
erative complications were not homogeneous among stud-
ies, and the time and accuracy of follow-up was not detailed
by most studies. This translates into a certain difficulty to
reach robust data on some long-term outcomes of interest,
such as anastomotic patency and the incidence of ascending
cholangitis.
Second, our search strategy included patients regardless
of age and indications for the index surgery (i.e. cholecys-
tectomy). As a result, the examined data may have been con-
founded at least in part, by the presence of both pediatric and
adult patients, as well as by the fact that the outcomes of pa-
tients receiving surgery for uncomplicated cholecystolithiasis
|
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may have been aggregated with those of patients undergoing
cholecystectomy for acute cholecystitis.
Finally, the specific technical experience of surgical teams
may have varied significantly among studies and over time,
as the included studies aggregate data coming from an inter-
val period greater than 25 years. Consequently, the outcomes
of MIS may have been biased significantly by the presence
of super-selected patients, especially at the beginning of each
experience.
5  |  CONCLUSIONS
Minimally invasive surgery is gaining acceptance in the man-
agement algorithm of cholecystectomy-related lesions of the
biliary tract. Both conventional laparoscopic and robotic re-
pair offer a valid option of treatment in referral centers with
specific experience.6,9,11 Even in the case of complex BDIs,
MIS may offer well-known advantages over conventional ce-
liotomy on surgical outcomes and abbreviated postoperative
convalescence.
To date, the absence of prospective studies and the risk
of selective bias precludes the possibility to define the ac-
tual role of MIS in the surgical management of BDIs due to
cholecystectomy. However, the results provided by a growing
number of highly specialized centers are encouraging and
warrant further investigation.
CONFLICT OF INTEREST
None declared.
AUTHOR CONTRIBUTIONS
All authors have contributed to the work in terms of concep-
tion and design, acquisition of data, analysis and interpreta-
tion of data. Francesco Guerra wrote the paper. All authors
contributed equally in revising the manuscript and approving
its final version.
ORCID
Francesco Guerra  https://orcid.org/0000-0003-2891-4659
Diego Coletta  https://orcid.org/0000-0002-9116-0733
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How to cite this article: Guerra F, Coletta D, Gavioli
M, Coco D, Patriti A. Minimally invasive surgery for
the management of major bile duct injury due to
cholecystectomy. J Hepatobiliary Pancreat Sci.
2020;27:157–163. https​://doi.org/10.1002/jhbp.710