MESTRADO INTEGRADO EM MEDICINA Iatrogenic bile duct injuries in the era of laparoscopic cholecystectomy Ana Margarida Ferreira Maia Gomes Cabral M 2018
MESTRADO INTEGRADO EM MEDICINA
Iatrogenic bile duct injuries in the era of laparoscopic cholecystectomy
Ana Margarida Ferreira Maia Gomes Cabral
M 2018
ARTIGO DE REVISÃO BIBLIOGRÁFICA
IATROGENIC BILE DUCT INJURIES IN THE ERA OF
LAPAROSCOPIC CHOLECYSTECTOMY
Dissertação de candidatura ao grau de Mestre em Medicina submetida ao Instituto de Ciências Biomédicas Abel Salazar da Universidade do Porto
Orientadora Mestre Donzília da Conceição Sousa da Silva Assistente Graduada de Cirurgia Geral da Unidade Hepato-biliar e Pancreática do Centro Hospitalar do Porto Professora Auxiliar Convidada do Instituto de Ciências Biomédicas Abel Salazar da Universidade do Porto Autora Ana Margarida Ferreira Maia Gomes Cabral [email protected] Maio de 2018
i
Resumo
Contexto: As lesões das vias biliares são um problema relevante na colecistectomia
laparoscópica, com um grande número de publicações dedicadas a este tema. Apesar de
todas as vantagens da abordagem laparoscópica, este procedimento ainda é marcado
pelo receio de lesão iatrogénica das vias biliares. Esta revisão pretende reunir o
conhecimento atual sobre esta matéria.
Métodos: Revisão de literatura sobre lesões das vias biliares em colecistectomias
laparoscópicas para analisar a sua incidência, classificação, demografia, causas e fatores
de risco, tratamento, mortalidade e uso de colangiografia intra-operatória. Grandes séries
(>1000 colecistectomias laparoscópicas) foram obtidas através de uma pesquisa na
PubMed. Outras referências foram encontradas a partir de artigos relevantes.
Resultados: foram encontradas 14 séries com mais de 1000 doentes que abordavam
lesões das vias biliares durante colecistectomias laparoscópicas, tratando o tema de
perspetivas diferentes.
Conclusão: a colecistectomia laparoscópica é uma cirurgia segura, mas os cirurgiões
devem ter em conta a possibilidade de lesão iatrogénica das vias biliares a qualquer
momento. A sua incidência é maior do que a incidência em colecistectomias por
laparotomia, mas a maioria das lesões não é complexa e pode ser tratada com sucesso.
Deve haver uma avaliação de fatores de risco antes da cirurgia para todos os doentes.
Os cirurgiões devem identificar as estruturas anatómicas com precisão. A colangiografia
intra-operatória é importante em certos casos, e os cirurgiões hepato-biliares são
essenciais no tratamento de lesões das vias biliares.
ii
Abstract
Background: Bile duct injury is a relevant problem in laparoscopic cholecystectomy, and a
gross body of literature has been dedicated to this topic. Despite all of the advantages of
the laparoscopic approach, this procedure is still marked by the fear of iatrogenic bile duct
injury. This review aims to be a state of the art on the subject.
Methods: Review of literature concerning bile duct injuries during laparoscopic
cholecystectomy to address its incidence, classification, demographics, causes and risk
factors, management, mortality and use of intraoperative cholangiography. Large series
(>1000 laparoscopic cholecystectomies) were extracted from a search through PubMed.
Other relevant references were obtained from main articles.
Results: 14 series with more than 1000 patients assessing bile duct injury during
laparoscopic cholecystectomy were found, each one addressing the injuries in a different
way.
Conclusion: Laparoscopic cholecystectomy is a safe procedure, but surgeons should keep
in mind the possibility of bile duct injury at any time. Incidence is higher than that of open
cholecystectomy, but most injuries are not complex and can be managed with success.
There should be a preoperative evaluation of risk factors for every patient. Surgeons must
recognize biliary anatomy accurately. Intraoperative cholangiography is important in
selected cases, and hepatobiliary surgeons are essential in the management of bile duct
injuries.
iii
List of abbreviations
BDI Bile Duct Injury
CT Computed Tomography
EAES The European Association of Endoscopic Surgery
ERCP Endoscopic Retrograde Cholangiopancreatography
ESGE European Society of Gastrointestinal Endoscopy
IOC Intraoperative Cholecystectomy
LC Laparoscopic Cholecystectomy
LUS Laparoscopic Ultrasonography
MRCP Magnetic Resonance Cholangiopancreatography
NBD Nasobiliary Drain
NIS Nationwide Inpatient Sample
OC Open Cholecystectomy
PRISMA Preferred Reporting Items for Systematic Reviews and Meta-
Analysis
PTC Percutaneous Transhepatic Cholangiography
RHA Right Hepatic Artery
US Ultrasound
iv
Index
Introduction 1
Methods 1
Results 2
Discussion 6
Figures 19
Tables 20
List of references 21
1
Introduction
The introduction of laparoscopic cholecystectomy (LC) more than 3 decades ago1
changed the way cholecystectomy is performed. This procedure started being increasingly
performed in the years that followed2 and it is now the standard method when removing
the gallbladder, having replaced traditional open cholecystectomy (OC). However, this
technique has been associated with an increase in the incidence of iatrogenic injuries to
the biliary tree.3
The rate of bile duct injury (BDI) was reported to be higher in the years following
the introduction of LC.4 This was proposed to be due a "learning curve" effect4, therefore,
it was expected to lower down as surgeons would get more experienced with the new
procedure.3 By that time, the rate was reported to be higher than the rate of BDI after
open cholecystectomy.5–8 Yet, some studies support that this rate remained higher.3,8–10
Stated by some as the most important cause of morbidity11, BDI after LC can be a
serious complication1, which may require complex management and have an effect on the
patient's quality of life.4 This review aims to review the incidence, classification,
demographics, causes and risk factors, management and results of BDI after LC.
Methods
Protocol
This systematic review was conducted following the guidelines set by the
Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA).
Elegibility criteria
Only full-text articles were included, published in English, Portuguese and Spanish
language. No restrictions were made regarding the time of publication.
Inclusion criteria for the systematic review were studies based on series of more
than 1000 patients who underwent elective or emergency laparoscopic cholecystectomies
reporting BDI incidence and other characteristics of BDIs, such as demographics, risk
factors, and management. Case reports were disregarded. Studies including observations
from both laparoscopic and open cholecystectomies were included, after ensuring each
procedure had its own separate data.
2
Search strategy
Two different searches were performed through PubMed on 8 February, 2018. The
key words "iatrogenic bile duct injury laparoscopic cholecystectomy" and "medical errors
bile duct injuries laparoscopic cholecystectomy" were used in order to identify the most
recent and the best matched articles published in literature, respectively. After screening
through publication titles and abstracts, full-text articles were reviewed according to the
inclusion criteria. Other relevant articles were found through reference lists of main
articles.
Results
The preliminary searches found 177 full-text papers potentially significant for this
review (figure 1). Additional records were identified through studies' reference lists (n=75).
After exclusion of replicates (n=4), non-English, -Portuguese or -Spanish papers (n=13),
studies not related to LC (n=9) and studies concerning species other than humans (n=2)
were excluded. 224 titles and abstracts were then assessed for eligibility, and there was
an exclusion of articles that did not share relevant information (n=83), were cases reports
(n=28) or were related to other species (n=4). It was not possible to access 1 study. The
inclusion criteria were applied to select studies in order to present and discuss big series
reporting LCs and BDIs. 18 articles were pertinent for this purpose, but some were based
on less than 1000 patients (n=4); therefore, according to the inclusion criteria, the results
of 4 studies were not presented and discussed. The other studies, which were not
excluded, were used as a basis to gain insight into the discussed topics and for review
purposes. In total, 107 studies were cited.
One prospective study by Richardson et al12 was based on 5913 LCs performed
from 1990 until 1995. From this group, information about 101 LCs is missing, but the
98,3% completed data was independently validated by 1 research nurse. A study by Veen
et al13 based on data collected prospectively from 1998 to 2006 reported 1254 LCs,
including 13 BDIs. The data extraction was described and additionally two not affiliated
authors evaluated all patient files for non-registered complications, and found another 2
cases of BDI.
A study by Grönroos et al14, based on 3736 LCs performed in a single institution
from 1995 to 2002, was conducted to identify if male gender was associated with BDI. It
did not describe the data extraction process but found 32 BDIs. A study by Karvonen et
al15 was based on the same database during the same period of time, therefore had the
3
same results and will not be discussed. Yet, the authors shared further data on mortality
and management of the patients, which will be included.
A retrospective study by Fullum et al16 analyzed a nationwide database, the
Nationwide Inpatient Sample (NIS), to find patients who underwent cholecystectomies (LC
and OC) from 1998 to 2006. The aim was to find patient and hospital factors potentially
associated with BDI. The factors were examined by use of bivariate and multivariate
analysis and included, among others, age, race, gender, morbid obesity, diagnosis of
acute cholecystitis, intraoperative cholangiography, year of procedure and hospital annual
volume of cholecystectomies. They found 177 BDIs in a total of 312522 LCs. Another
retrospective study, by Aziz et al,17, which had the same goal, used records from the
same database, but analyzed data from 2010 until 2012 concerning 39844 LCs, and
found 177 BDIs. Univariate and multivariate analysis were perfomed to find association
between the same factors and BDI. One study was based on the same database on the
same period of time as the one by Fullum et al16, therefore it is not discussed, as it would
be a replica.
A retrospective multicenter study by Savassi-Rocha et al18 described 91232 LCs
performed from 1990 until 1997. It found 167 BDIs and a further 83 cystic duct injuries
which were not included in the analysis. Another retrospective single institution study by
Tantia et al19 was based on data recorded for 13 consecutive years, from 1992 to 2005.
A retrospective study by Demartines et al1 reported BDI after LC based on data
from 11 year experience, from 2000 until 2011, from a single-institution.
A multicenter retrospective by Malik et al20 analyzed 1132 LCs performed from
2003 to 2007 and found 19 BDIs, plus 13 minor postoperative bile leaks which resolved
spontaneously and were not included in the analysis.
A multicenter retrospective study by Hamad et al21 extracted data from patients
undergoing LC between 2004 and 2009, selecting only cases where IOC had not been
used, thus excluding the ones where surgeons had resorted to this procedure (a "no-
intraoperative cholangiography policy"). There is a concern that this lead to a selection
bias, where mostly not so complex LCs, that did not require cholangiography at the time
they were performed, would be included. Therefore, their results are not included in this
review. A survey by Paczyński et al22 analyzed 6873 patients who underwent LC from
1991 until 2000. It did not describe how data was extracted or discuss its own results.
Hence, this survey is not presented in this review. A study by Suliman and Palade23
reported 1402 LCs in patients suffering from acute cholecystitis. It addresses mostly
problems encountered in this disease and does not provide the information needed for
this review, therefore their results are not discussed.
4
Incidence of BDI
All of the studies reported the incidence of BDI caused by LC. The rate was found
to range between 0,06%16 and 2,55%17.
Among the earlier series, Richardson et al12 and Savassi-Rocha et al18 (1990-1995
and 1990-1997) reported an incidence of 0,63% and 0,18%, respectively. Grönroos et al14
(1995-2002) reported an increase of the rate up to 0,86%. Concerning the first half of the
2000s (1998-2006), Veen et al13 and Fullum et al16 stated that the incidence was 1,20%
and 0,06%, respectively. From 2003 to 2007, Malik et al20 reported a rate of 1,68%. The
highest value was found in the most recent study (2010-2012), by Aziz et al17, which
reported a rate of BDI of 2,55%.
Tantia et al19 and Demartines et al1, based on data from 13 and 11 consecutive
years from single institutions (1992-2005 and 2000-2011), reported a rate of 0,39% and
0,46%, respectively.
Classification of BDI
Only two studies used the Strasberg-Bismuth classification. Tantia et al19 reported
that the most frequent injuries were Strasberg type A and type D (27 and 14 out of 52
BDIs). When these were excluded, most of the BDIs occurred in the middle CHD and
identified as E (2 E1, 3 E2 and 1 E3 injuries). 32 were identified intraoperatively.19
Demartines et al1 reported that, out of 13 BDIs, the most frequent injuries were Strasberg
type A, 4, and D, also 4, followed by E1, 3, and E5, 2. 6 injuries were identified
intraoperatively.
Veen et al13 used the Strasberg classification. Out of 13 injuries, 8 classified as
Strasberg type A, 4 as type D and 1 as type E. The study also reported 1 additional bile
leak from the cystic duct and 1 lateral injury of the common bile duct.
Savassi-Rocha et al18 applied the Bismuth classification to 158 out of the 167
BDIs. The most frequent were type 1 injuries, 107, followed by 41 type 2 lesions, 9 type 3
and 1 type 4 injury. The other 9 BDIs were reported to be isolated injuries of the right
hepatic duct. 113 injuries were discovered during the procedure. They also reported 83
cystic duct injuries.
Grönroos et al14 used the Amsterdam Criteria. They report 10 type A, 5 type B, 8
type C and 9 type D injuries. Other 2 studies used different systems and 2 did not specify
the types of BDI suffered by the patients.
Richardson et al12 used the McMahon classification and considered 20 injuries as
major, which included 9 lacerations of the CBD, 8 injuries of the CHD including significant
trauma to the confluence, 1 right hepatic ductal laceration and 2 strictures at the cystic
duct insertion. The other 17 were considered minor and comprised 9 small lacerations in
5
the CBD, 6 lacerations of the CHD and 2 of the RHD. From the 37 injuries, 18 were
detected during the procedure while 19 were found in the postoperative period.
Malik et al20 comprised 3 transections of aberrant RHD, 7 partial injuries to major
biliary ducts, 5 accidental holes in CBD, 1 CBD mistakenly clipped and not recognized, 1
CBD clipped in place of cystic duct but recognized immediately and 2 accidental holes in
the CHD. 7 injuries were identified intraoperatively.
No studies mention concomitant vascular injuries.
Patient gender
Only 4 studies1,14,17,19 mention the gender of patients who sustained BDI.
Demartines et al1 reports 7 BDIs occurred in females and 6 in males. On another
two studies14,19, BDIs occurred mostly in females (25 vs. 7 males14 and 32 vs. 20 males19).
However, in one of these studies the authors concluded male gender seemed to be
associated with BDI19 and the other found no statistically difference in the risk of BDI14
between males and females. Aziz et al17 showed male gender was associated with CBD
injury in a univariate model but it was nonsignificant in a multivariate analysis.
Causes and risk factors for BDI
When reported, the most frequent cause of BDI in the studies1,12,20 was anatomical
misunderstanding, specifically misinterpreting the common bile duct with the cystic duct.
Some studies18,20 refer risk factors for BDI. Besides male gender16,17,19, the most
mentioned risk factors were local inflammation and acute cholecystitis, older age (>65
years), anatomical abnormalities, chronic cholecystitis, using a 0º laparoscope,
hemorrhage, emergent cholecystectomy and obesity.12,16,17,19,20 Karvonen et al15 refers to
acute and chronic cholecystitis as a frequent technical problem. Fullum et al16 did not find
acute cholecystitis associated with BDI, but it increased mortality.
Management of BDIs
Seven studies mention BDI management1,15–20. Three separate the management
of lesions by the time of its recognition (intraoperative and postoperative) and type of
lesion1,18,19. The most frequent procedures when dealing with intraoperative diagnosis
were suture by laparoscopy or conversion to laparotomy (end-to-end anastomosis and
Roux-en-Y hepaticojejunostomy). When the recognition was made after the LC, patients
were mostly treated by percutaneous drainage, stenting by endoscopic retrograde
cholangiopancreatography (ERCP), sphincterotomy and laparotomy for biliodigestive
anastomosis.
6
Karvonen et al15 didn't specify the time of diagnosis but described management by
type of BDI lesion by Amsterdam criteria. Type A lesions were treated endoscopically, the
majority by sphincterotomy and biliary stenting. Most type B underwent laparotomy (2
immediately, 2 later) mostly for a T-tube suturing or endoscopic stent. Type C lesions
were mostly treated by endoscopic measures (dilatation and stenting). The majority of
patients who sustained type D injuries underwent hepaticojejunostomy or
cholangiojejunostomy.
One study20 mentioned T-tube repair, primary suture and suture ligation as the
most frequent procedures for BDI repairing. Two studies16,17 mention only ICD codes and
do not specify their frequency. Nevertheless, the procedures include simple suture of
CBD, biliodigestive anastomosis, ERCP, choledochoplasty and repair of other bile ducts.
Mortality related to BDI
Only 6 studies1,12,15,18–20 reported mortality related to BDIs. Savassi-Rocha et al18
reported a 4,2% rate (7 deaths out of 167 patients), Karvonen et al15 reported a 3,1% rate
(1 out of 32 patients) and Malik et al20 a 5,3% rate (1 out of 19). Demartines et al1,
Richardson et al12 and Tantia et al19 reported no deaths.
Intraoperative cholangiography to identify IOC
Demartines et al1 reported routine use of IOC until 2006. From the 13 BDIs, IOC
was performed in 8 patients and helped identify 3 injuries, confirmed a suspected BDI in 3
cases and was misinterpreted (as normal) in 2 cases. Savassi-Rocha et al18 reported
routine IOC allowed the surgeons to identify 19,5% of BDIs. When this exam was only
selectively performed, 28,3% of BDIs were identified.
Richardson et al12 reported selective use of IOC and authors referred that IOC was
not important in the identification of BDI.
Other studies that mention IOC performed it in selected cases only13,14,19 or did not
provide full information related to this procedure16,17.
Discussion
Biliary duct injury has been proposed as the most serious and potentially life-
threatening complication of cholecystectomy.24
Since the implementation of LC, studies have shown an increased rate of this type
of surgery2,25,26. In 1993, the NIH Consensus conference considered it a safe and effective
treatment for most patients with symptomatic gallstones and it remains the treatment of
7
choice for many patients since.27,28 Cholecystectomy is nowadays one of the most
commonly performed abdominal surgeries and, in the USA, 90% are performed
laparoscopically.29 LC results in less postoperative pain, faster recovery and shorter
hospital stay and has less impact on physical appearance than OC.30–32
A considerable disadvantage of this procedure has been the incidence of
BDIs4,5,20, which is proclaimed by some to have increased as a "learning curve" effect but
has remained high even after that period of time3,4,20. Some studies state the incidence of
BDI has increased from 0,2 to 0,5% from its debut to its regular use and, accordingly, it is
higher than BDI after OC.4,8,33 This is contradicted by other studies that report an
improvement of this rate over the last years.34,35
Although its incidence is, nevertheless, low, BDIs increase morbidity and mortality
and decrease the quality of life of patients, specially the patient’s mental health36–39.
Awareness of this important repercussion turns mechanisms for its prevention,
identification and treatment very important. Studies have been made to define risk factors
for BDI after LC, including (but not limited to) obesity, age, male gender, severe
inflammation or infection and surgeon’s experience.4,14,16,17,29 After injury has occurred,
management will depend on the type and extent of BDI and timing of its diagnosis. Early
referral to a tertiary center for a multidisciplinary approach seems to be important.40,41
Incidence
Over the decades after LC started being used, a lot of studies have reported BDI
incidence, which has been varying considerably. Among the first larger series published,
Deziel et al5 reported a 0,60% BDI rate after 77604 LC and MacFadyen et al7 a 0,50%
incidence of major BDI in a total of 112532 cases. The fact that both studies exclude
cystic duct injuries may underestimate BDI. In 1960, Rosenqvist and Myrin figured that the
incidence of BDI after the traditional OC in Sweden would vary between 0,25-0,33%,
Madsen et al estimated an incidence of 0,31% in Denmark and Viikari a 0,20% incidence
in Finland.42 These large series agree with the vast body of literature that has reported LC
was associated to a higher BDI incidence than OC during the first years after it started
being used.
In this review, the overall incidence of 0,63% reported by Richardson et al12
between 1990 and 1995 support the previously mentioned LC series. The incidence
peaked at 0,80%, but it should be mentioned that this value fell to 0,40% in 1995. In
contrast, Savassi-Rocha et al18 report a lower incidence, harmonious with OC rates, but
they exclude cystic duct injuries. If included, they would increase the incidence of BDI to
0,27%. This rate would still be comparatively low, but one should be careful in comparing
these 2 studies. Although Savassi-Rocha et al18 was conducted between 1990 and 1997,
8
more than 80% of units had already performed more than 100 operations at the time of
the survey (almost 40% had performed more than 500 LCs) and Richardson et al12
include data since this type of procedure was launched in the West of Scotland hospitals.
Analyzing the studies included in this review, it appears that, as time went by, the
incidence of BDI increased. Grönroos et al14 reported a rate of 0,86% and Veen et al13
1,20%. It should be taken into consideration that the majority of injuries reported in both
studies were type A Amsterdam criteria (leakage from the cystic duct or peripheral hepatic
radicals) or type A Strasberg (bile leak from cystic duct or liver bed without further injury),
which can be relatively easily treated.
Malik et al20 report a BDI incidence of 1,68%. Among the 19 BDIs, 1 injury was
clipping of the CBD instead of the cystic duct, which was recognized and removed
immediately. The authors discussed that, in their experience, majority of injuries could be
avoided by simple measures like lowering the threshold for conversion to OC when
identification of anatomical parts is difficult. They also concluded surgeon's over-
confidence and casual attitude in operating rooms should be further evaluated. They do
not report the rate of conversion in the study, so it is not possible to conclude if it was
lower than other series.
On the other hand, Fullum et al16 report an overall incidence of 0,06%. They could
not account for BDIs in patients who were diagnosed after discharge (important aspect
since the length of stay is shorter for LC than OC), only if they were still hospitalized.
Furthermore, they could not include LCs where a BDI was noticed and the procedure was
converted to an open approach for repair, as it would be coded in the database as an OC.
They also report a decrease of BDI incidence after all cholecystectomies (laparoscopic
and open procedure). This is important because the rate of OCs decreased from 19,5% in
the initial 3 years of the study to 15,1% in the last 3 years.
The two longest studies1,19 report similar BDI incidence (0,39% and 0,46%) even
though they differ on the time period they comprised. This is an overall rate and, as such,
one cannot realize if BDI actually increased or not.
Aziz et al17 report a rate of 2,55%. This value is completely different from what one
can find in most literature. It is worth mentioning that, in this study, acute cholecystitis
represented 41% of the pathologies requiring LCs, which has been proposed by some as
a risk factor for BDI in LCs. Emergent LCs represented 61% of the total number of LCs,
which has also been proposed as a risk factor for conversion to OC and adverse
outcome43,44. The authors also explained that the database made preexisting comorbid
factors difficult to separate from postoperative complications.
Browsing the literature, one can find that a substantial number of studies cite an
incidence of BDI after OC of 0,1 to 0,2%. As mentioned before, some older studies report
9
rates between 0,20 and 0,33%42. Additionally, in a large series of 36278 surgeries, Waage
et al4 report an incidence of 0,40% in the years preceding the introduction of LCs (1987 to
1990). Similarly, Diamantis et al34 report a 0,38% incidence of BDI after OCs between
1991 and 2001. Therefore, it can be inaccurate to assume that the incidence of BDI after
OC is as low as it has been stated in literature, as it may differ. Other important aspect is
that, in older OC series, like the ones discussed previously, the same definitions of BDI
may not have been rigorously applied. Another condition to consider, when reading any
study, is the frequent selection bias; patients who undergo OC may be different from the
ones undergoing LC.
Although the incidence of BDI after LC appears to have been higher during the first
years, it is difficult to define a specific value for its incidence after reading the studies
presented here as the rates vary greatly. The patients included in the studies, the
methodology, access to databases and follow-up information differ considerably. In this
review, the largest series have lower rates of BDI incidence. Considering the conditions of
each study and the incidence of BDI after OCs mentioned previously, it appears that BDI
incidence after LC is found to be slightly higher than that of OC. One can realize it is,
anyway, a very low value.
Classification of BDI
Several classifications have been used to help describe the injuries, the most used
being Bismuth and Strasberg classifications. The categories are an useful tool to the
surgeon since they help in choosing the most adequate management procedure to repair
the injury and to compare their outcomes.45,46
Proposed in 1982, in the era of open cholecystectomy, the Bismuth classification
has since been widely used.45 It is based on the level of the injury, at which non-damaged
bile ducts are available for anastomosis, and is known to have a good correlation with the
outcome after injury management.46,47 It divides BDIs into five types (table I).45
With the onset of LC, the Bismuth classification was not able to include the range
of BDIs that could possibly develop. Isolated right hepatic duct strictures, other strictures
and leakage from the cystic duct could not fit into this system. In 1995, the Strasberg
classification expanded on the Bismuth classification and brought new categories that
could be applied to those injuries (table II).47,48 Therefore, the Strasberg-Bismuth
classification includes types A to E and allows differentiation between small and severe
injuries. Type E BDIs are subdivided into E1 to E5 under the Bismuth classification.
Although it can be easily applied, it does not express possible vascular engagement.49
Also in 1995, McMahon et al50 proposed a classification of minor or major injury
based on the width of BDI. Laceration under 25% of the bile duct diameter or buttonhole
10
tear were classified as minor, and laceration of over 25% (or transection) of CHD or CBD
or postoperative stricture were classified as major injuries. In 1996, the Amsterdam
Academic Medical Center's classification was proposed by Bergman et al (table III). It
divides injures from type A to type D.51
Other classifications have been suggested, like the ones proposed by Olsen
(1997)52, Martin et al53, Neuhaus et al45 (2000), Csendes et al (2001)54, Stewart et al
(2004)55 and Lau et al (CUHK classification) (2007)46. The last 2 include vascular
injuries.46
Bektas et al proposed the Hannover classification in 2007.56 It includes vascular
injuries, has determinants for the location of the damage and demonstrates an association
between BDI pattern and surgical repair and also with the resection of liver tissue and
hepatic duct bifurcation.45
The studies included in this review use different BDI classifications. For that
reason, it is difficult to bring together all their results. One can observe that the most
frequent type of injury found was Strasberg type A or "cystic duct injuries".1,13,14,18,19 This
reflects the trend reported by other studies.5,57 Hence, although the incidence of BDI found
in some studies was higher than what one would expect, the majority of injuries inflicted
were minor BDIs. In these cases, the bile ducts are in continuity with the biliary tree, which
allows a possibly easy management.58 Type D injury was the second most frequent
injury.1,18,19 In this type, the continuity of the biliary duct is kept as well, and its repair will
depend on the vascularization of the duct.
Some studies1,13,18,19 also report type E lesions, with Savassi-Rocha et al reporting
a majority of Bismuth types 1 and 2. Type 1 is an anatomically low injury which can be
treated without lowering the hilar plate46. On the other hand, under the McMahon
classification, the majority of lesions reported by Richardson et al were considered major,
but the number was almost equal to the minor injuries.12 Still, this is an older study and the
learning curve period may have an impact on the severity of the lesions. The authors also
refer that if only major BDI is included, the rate would be comparable to retrospective OC
series.12 In spite of the results of these studies, a prospective study by Dorcaratto et al59
concluded that BDI occurring during LCs is becoming more complex as surgeons perform
more difficult LCs, and vascular injuries are becoming more common.
The incidence of vascular injuries found in literature varies greatly. While in a
series of autopsies Halasz et al60 reported a 7% incidence of arterial injury in patients that
had sustained OC, Alves et al61 reported a 47% incidence of vascular injury in patients
who had suffered BDI during LC. This is understandable, specially, after realizing that the
most affected vessel is the right hepatic artery (RHA)55,61,62, because as BDI due to LC are
more proximal in the biliary tree, they get closer to the location of the RHA55. Yet, Alves et
11
al61 mention a series of OCs where routine angiography was carried out and referred that
the authors found an incidence of vascular injuries of 39%. Regarding the present review,
one can not draw any conclusion since the studies did not mention these injuries nor used
a classification that included these types of injuries.
Studies have also reported that outcome is worse in patients who have a BDI with
a concomitant vascular injury compared to patients with BDI only, with a higher incidence
of abscess, hemobilia and hepatic ischemia and resection.55,63 Bilge et al62 found that the
frequency of complex BDI was higher when there was a concomitant vascular injury, but
concluded it had no significant effect on mortality and BDI repair. While an injury that
damages the blood supply of the ducts can cause complications due to local ischemia,
unilateral injury to the hepatic blood vessels, usually, does not cause complications, and
may therefore remain undetected, because blood can circulate via the hilar plexus. This
could explain why the management is comparably successful in patients with and without
vascular injury, particularly with a Hepp–Couinaud approach.61 Hence, Bilge et al62 did not
recommend routine use of angiography. Alves et al61 justified their high incidence with the
routine use of angiography, but added that it had no impact on the presentation of the BDI
or on treatment failure.
Patient gender
Male gender has been proposed as a risk factor for adverse outcomes in LC.64 In a
systematic review, Hu et al43 verified that male gender was considered a risk factor for
conversion to open procedure in several studies. Waage et al4 also found that male
gender was associated with a bigger risk of BDI in cholecystectomy. Kanakala et al44 also
found male gender was a predictor of morbidity, mortality and conversion to laparotomy
and proposed that they have a higher threshold of pain, are older and present later as
they have a more delayed presentation of disease. On the other hand, Kumar et al65 did
not find male gender statistically significant as a risk factor for BDI during LC.
In this review, the data concerning patient's gender, available in 4 studies, shows
that most BDIs occurred in female rather than male patients. In one of those studies,
Grönroos et al14 concluded that female gender is a risk factor for severe BDI in LC, but
they did not find statistically significant the difference in risk. Aziz et al17 showed male
gender was associated with CBD injury in an univariate model, but it was revealed to be
nonsignificant in a multivariate analysis. Tantia et al19 concluded male gender may
increase the chances of BDI. Hence, these studies do not dispute the literature that
supports male gender as a risk factor for adverse outcome in LC.
12
Causes and risk factors
In literature, one can find several factors associated with an increased risk of poor
outcome, conversion to OC and BDI, including male sex, age, obesity, acute cholecystitis,
comorbidities and emergency laparoscopy.43,44 It is frequent to find acute cholecystitis,
emergency LC and surgeon's narrow experience with LCs associated with BDI.8,66,67
When comparing literature with the results seen in the studies here included, it is not
surprising that the most mentioned cause of BDI was misidentification of CBD as the
cystic duct (the "classic injury"). Shallaly and Cuschieri47 highlight that these injuries could
be avoided if the surgeon identifies with certainty every anatomical struture. Other
anatomical mechanisms found in literature include lateral clipping of the CBD, traumatic
avulsion of the cystic duct junction and injury by diathermy of the CBD while dissecting
Calot's triangle.24
Inflammation was also a frequent mentioned cause, which is supported by
literature68. One can conclude that situations that further complicate LCs are indeed
causes that facilitate BDI. Nuzzo et al8 found that BDI associated with cholecystitis
occurred more in surgical teams with greater experience. These stress the importance of
evaluating risk factors and taking caution intraoperatively.
Mortality after BDI
Most mortality rates related to BDI in the series here included15,18,20 are slightly
higher that the ones presented in other studies7,40,41. Sicklick et al41 reported 1,7%
mortality early after definitive repair procedures, 1,5% due to sepsis (without a repair
procedure) and De Reuver et al40 found it to be 2,4%. Flum et al69 found that BDI
increased the likelihood of death within 10 years by 3 times. These studies40,41,69 highlight
the importance of tertiary center referral after BDI.
Management of BDI
The management of BDI is determined by the time of diagnosis and the type and
extent of the injury. An early diagnosis of BDI is important as it can avoid complex repair
procedures and complications like infection and fibrosis.70 Different studies33,51,71 have
recognized that only a minority of injuries, usually less than 30%, is recognized during the
initial procedure. In the studies presented in this review, the proportion of injuries detected
intraoperatively was almost equal1,12 or even higher18,19 than the ones detected
postoperatively. However, some injuries may present months or years after surgery48,
which means rates can change with long-term follow-up.
The success of repair is associated with a complete assessment of the anatomic
area involved before an attempt to repair the injury.72 Stewart et al72 reported that 96% of
13
BDI repairs were unsuccessful when cholangiograms were not obtained preoperatively,
but, when data was complete, 84% were successful. Thus, the anatomical area should be
investigated and the procedure for reconstruction should be carried out by a specialist
with experience in these procedures in order to achieve the best results72. Usually the
repairs are conducted best if other surgeon, different than the one who performed the first
LC, performs the repair.33
BDI recognized during the LC
BDI can be recognized directly, by intraoperative cholangiogram, or suspected by
the leakage of bile. If recognized, the surgeon should assess its severity and look out for
vascular injuries. He has to decide whether to repair it immediately or to refer the patient
to a specialist surgeon. Some BDIs, like cystic duct and gallbladder bed leaks and partial
duct lacerations, can possibly be managed right away by the surgeon, but this will depend
on their training and skills72. In the studies included in this review, while Demartines et al1
converted to laparotomy half of the cases diagnosed intraoperatively, Savassi-Rocha et
al18 showed a greater frequency of conversion to laparotomy. Tantia et al19 performed the
immediate repairs by laparotomy if there was a complete transection of a duct, but did
mostly by laparoscopy if the injury was lateral or sectorial.
Referral to a specialist surgeon with experience in BDI repair improves
prognosis72,73, and the patients' best interests should be kept in mind. If a biliary specialist
is needed but not available, a subhepatic drain can be placed and referral to an
hepatobiliary unit should be made as soon as possible.33 The European Association for
Endoscopic Surgery (EAES) guidelines suggest that a conversion to OC should only be
made by a biliary specialist after the confirmation of injury or to control hemorrhage in
cases of severe bleeding.74 The EAES recommend all injuries should be referred, except
leakage from cystic ducts or from the liver bed, which can be treated endoscopically.74
Additionally to bile leakage or hemorrhage, there are signs that may help suspect
a BDI will occur, like apparent ductal or anatomical abnormalities (may indicate the CBD is
being dissected instead of the cystic duct), an extra bile duct (could be the CBD or a
transected CHD), cholangiographic abnormalities (cholangiocatheter positioned in the
CBD) or a large artery posterior to the cystic duct (could be the RHA and actually the
CBD).33 Thus, a surgeon should keep in mind at all times the event of BDI in LC.
Archer et al75 reported that BDIs were more likely to be discovered during surgery
when a cholangiogram was obtained. The EAES guidelines state IOC and laparoscopic
ultrasonography (LUS) bring valuable information to the surgeon and advocate its use
when there are concerns about the biliary tree anatomy.74 IOC can detect CBD stones70
and find BDIs if they occur and LUS may also allow earlier recognition and their repair.76
14
BDI recognized postoperatively
Reviews and studies33,51,52,77 have reported the majority of BDIs are diagnosed
postoperatively. The main 2 injury types are bile leaks and biliary obstructions, which can
occur at the same time. As recovery from LC is frequently easy, the presence of BDI
should be investigated when the patient has symptoms that do not improve over time.33,74
Bile leaks usually present within the first few days or weeks after LC with vague
and mild symptoms, including a feeling of abdominal fullness, nausea, vomiting, fever,
and possibly abdominal pain.64 They usually do not cause severe peritoneal irritation64,
but can ultimately lead to bilomas, biliary fistulas, cholangitis or sepsis41, although bile
peritonitis with extreme manifestations is uncommon early after surgery even with large
amounts of bile77. Liver enzymes and bilirubin are usually normal.33,77 Hence, the
diagnosis can be difficult to establish. Lee et al77 reported bile collections were initially
missed in 77% of patients with BDI after LC as the clinical picture was nonspecific, and
the mean time to the diagnosis was 16,8 days. This is of utmost importance as they also
reported that later bile drainage (more than 10 days after LC) was associated with a
higher incidence of severe illness and positive bile cultures.77 Because bile can
accumulate even when a drain is placed at the time of the cholecystectomy, imaging
studies should be requested when there is a suspicion of BDI, that is, when the recovery
of LC is not smooth.77 Some studies report that, in the first days after LC, a small
collection of fluid can be found at the gallblader fossa.78,79
The presentation of obstruction is usually one of jaundice, anorexia, and
abdominal pain. Laboratory analysis may also show a cholestatic pattern.51,64 Studies
have reported alanine aminotransferase and alkaline phosphatase levels can be elevated
in the first days after LC, possibly because of the pneumoperitoneum inherent to the
procedure, but these are clinically insignificant and do not predict complications.80,81 In a
partial occlusion, the parameters of cholestasis can also decrease to the normal range
after 10 days.74 Biliary strictures can take months or years to develop and, when present,
can cause cholangitis, jaundice and cirrhosis.41
The EAES reccomend the use of computed tomography (CT) scan or ultrasound
(US) as the first choice to search for intra-abdominal bile collections and ductal
dilatations.74 These methods can detect fluid collections although they do not distinguish
the type of fluid present or its continuity with the biliary tree.82 Chole-scintigraphy scans
can detect an active bile leak but they have some disadvantages, like poor anatomical
definition, and consequently they become dependent on another imaging procedure.82 If
bile collections are present, they should be drained and cholangiography should be done
to visualize the ducts.74 ERCP can be therapeutic (allows for stenting or dilatation)82 and is
15
the recommended procedure.74 Percutaneous transhepatic cholangiography (PTC) or
magnetic resonance cholangiopancreatography (MRCP) are useful when a complete
obstruction is present, as ERCP won't be able to visualize the proximal biliary ducts in
such case.74,82 PTC also allows for dilatation and stenting and can help in decompressing
the proximal biliary tree.74,83 MRCP can be better in the diagnosis and can help choosing
the best management procedure, but has also some disadvantages.82,84
As in the case of BDI diagnosed during LC, concomitant vascular injuries should
be searched for because they can change the management strategy. Duplex US has
been referred as a non-reliable method to access these lesions, making room for
angiography.85 MRCP with hepatobiliary contrast material can provide this information.82
Besides the complete assessment before attempting to repair an injury and the
experience of the surgeon, the success of BDI management also correlates with the
elimination of abdominal infection and the use of an adequate surgical technique.73
Therefore, another goal before pursuing BDI repair is to control peritonitis or sepsis if they
are present.64,83 Electrolyte and nutritional status should be corrected and fat-soluble
vitamins supplemented.64 Although one can find literature supporting a waiting period of
time for repairing the BDI in order to decrease inflammation83, like 2 to 3 months64, a
multivariate analysis by Stewart et al73 concluded that timing does not correlate with the
success of management, hence there is no reason to delay it when all of these conditions
meet.
The management can be done endoscopically or surgically. Small injuries like
cystic stump or accessory bile duct leaks can be treated endoscopically with stenting and
drainage of collections, insertion of a nasobiliary drain (NBD) or sphincterotomy.86–88
Stenting and sphincterotomy are done to allow better flow of bile to the duodenum and
decrease its pressure inside the ducts, allowing the injury to heal, and can be done
together.88 NBDs decrease pressure inside the biliary tree and allow further
cholangiographies but can be uncomfortable, can dislodge and the patient is compelled to
stay hospitalized until they are removed.89 Although the endoscopic procedures have
been shown to be safe86,89–91, there are no studies comparing these procedures. Kaffes et
al92 concluded that stenting was superior to sphincterotomy, but one can point out some
limitations in the study93. In a series of 207 patients, Sandha et al88 applied different
approaches for high and low grade bile leaks with good outcomes. It is known that
stenosis can occur after the stent is removed71 and that sphincterotomy carries a risk of
acute and long-term complications94. In the absence of lesions, like a retained stone, the
EAES and the European Society of Gastrointestinal Endoscopy (ESGE) advocate stenting
should be done without sphincterotomy74,95. When removing stents, Pioche and
16
Ponchon70 advise execution of new cholangiograms in order to guarantee the ducts are
free of obstructions.70
Bile duct strictures can also be repaired with endoscopic stenting.51,87,89,96 Studies
support that it can be an alternative to hepaticojejunostomy96 and that the use of multiple
stents can improve outcomes97. While the rate of recurrent stricture was found to be
around 20% after 2 years in a study98, Costamagna et al97 reported no cases of
recurrence with the use of a more aggressive approach (up to 6 stents). In the case of
strictures, the ESGE recommends the use of temporary stents.95 In any of the approaches
mentioned before, the advantages and disadvantages of each procedure should also be
discussed with the patients95. If the endoscopic approach fails, then hepaticojejunostomy
can be performed. In a study99 concerning OC patients, early complications were found to
be more common in the surgically treated patients, while there were more late
complications in the endoscopically managed patients (including stent migration) and both
strategies had similar success rates.
Partial bile duct lacerations recognized at the LC can be repaired with simple
suture repair and drainage.51,71,83 Some authors advocate suture over a T-tube64, while
others state that it can enlarge the laceration and later evolve into a stricture33.
Discontinuity with the bowel will require a surgical approach.64 In the case of a complete
transection (or a large laceration) of the CBD or CHD, there can be more loss of tissue
and it is more likely that the biliary microvasculature could be damaged71,83. A primary
end-to-end anastomosis has been shown to be unsuccessful in these cases as it will
frequently be under tension, even with mobilization of the duodenum, in combination with
the possible decrease in blood supply, and later evolve into a stricture.64,72 Savassi-Rocha
et al18 showed end-to-end anastomosis was performed in 26,3% of BDIs, but authors
stressed the importance of long follow-up in order to identify late complications, such as
strictures. In the majority of cases, a Roux-en-Y hepaticojejunostomy is the preferred
procedure,71,83 and the Hepp-Couinaud approach can be of particular interest for injuries
where the confluence is intact.64 As mentioned before, if there is no specialist surgeon
available at the time of the LC, drains should be placed and the patient referred to a
specialized unit.
In general, the studies in this review which address BDI management1,15,18,19 and
follow-up adopted these principles. None concluded if any therapy was superior to any
other. Demartines et al1 performed stenting as a first line treatment, when possible,
followed by surgical repair if the first one failed, and reported good results, without the
need of liver resection or transplant. As a therapy for stenosis, Savassi-Rocha et al18 did
not conclude which type of repair was better, but highlights that, in tertiary referral centers,
surgical management achieved a 96% success rate. At the time of the survey, they
17
reported 87,4% patients were asymptomatic.18 In the study by Karvonen et al15, only 1
patient suffering from stricture (12%) required hepaticojejunostomy after endoscopic
treatment. Tantia et al19 reported only 2 patients (3,85%) had recurrent symptoms
(cholangitis) after treatment in a 24-month follow-up. These findings in different studies
support the management strategies mentioned before.
Hepatic or sectoral duct injuries can be difficult to detect. A cholangiography may
seem normal because of the absence of contrast leakage and the presence of a normal
right and left ducts' confluence.83 There is also the possibility of anatomic variations of the
biliary tree, which would make it harder to correctly identify the biliary ducts during LC.71
The resulting biliary leakage should be drained in order to avoid development of more
severe conditions and elective surgical repairing of the injured duct done by a specialized
surgeon as a Roux-en-Y hepaticojejunostomy.100 Although the Hepp-Couinaud approach
is useful for left sided injuries, some studies101,102 used this method to right sided injuries
as well, with good results. If these approaches fail, then liver resection can be
envisaged.83
In a review, Tzovaras and Dervenis103 refer vascular injuries during LCs have been
associated with bleeding, difficult BDI repair and strictures. The most frequent injured
blood vessel during LC is the RHA, which is usually lying posteriorly to the CHD.103
Because of the architecture of the hepatic circulation, an injury to the RHA can remain
unnoticed.71,83 Some authors even suggest not to repair this injury because it rarely has
consequences, if the liver is otherwise healthy.64,103 With an associated bile duct injury,
some state BDI can be repaired without the reconstruction of the artery.55 Others highlight
the possible liver atrophy and necrosis, which would need resection or
transplantation104,105.
Intraoperative Cholangiography
In addition to showing the biliary tract anatomy and detecting CBD stones, IOC
can help recognize BDIs.70 However, its routine use is controversial because of the lack of
randomized studies reporting a decrease in BDI incidence in this scenario. IOC increases
LC time and costs, and is susceptible to error, like incision of the CBD instead of the cystic
duct, which could itself lead to an injury.70 Even in this case, the IOC could help identify
this injury, if it would be interpreted in the correct way by the surgeon. In the series by
Demartines et al1 it was reported that IOC provided BDI identification in 3 out of 8 BDIs,
but other 2 IOCs were interpreted as normal when, in fact, there was an injury. Some
studies report an association between performing routine IOC and a decrease in BDI106,
but in order to understand if there is a causal relationship between these factors then
variables, confounders and effect modifiers should be taken into account.107
18
In this review, Savassi-Rocha et al18 reported 19,5% of BDIs were identified
because IOC was routinely performed. Yet, they also mention that 47,8% of the BDIs
were identified before the actual routine IOC took place. This means that, when it was
routinely used, 66,7% of BDIs were identified prior to the procedure. The authors
concluded that the majority of diagnoses were made without the use of IOC.
While there are no studies exploring this subject, it appears that the best conduct
is to make use of an adequate surgical technique and decide whether to perform IOC or
not as already mentioned by the EAES74. It is important to stress that IOC cannot prevent,
by itself, a BDI.107
Conclusion
Bile duct injury is one of the most relevant problems of laparoscopic
cholecystectomy. Its incidence appears to have remained slightly higher than in the era of
open cholecystectomy, but most injuries are not complex, and most patients experience
resolution of symptoms after proper management. Risk factors should be considered
before surgery. The most frequent cause for BDI was misunderstanding anatomical
structures, something surgeons should keep in mind. Surgical management should be
done by experienced surgeons in specialized units. Routine intraoperative
cholangiography is a matter of debate but appeared not to be important.
19
Figures
Figure 1. PRISMA flow diagram.
20
Tables
Table I. Bismuth's classification of bile duct injury
Type Criteria
1 Low CHD stricture, with a length of the common hepatic duct stump of >2 cm
2 Proximal CHD stricture-hepatic duct stump <2 cm
3 Hilar stricture, no residual CHD, but the hepatic ductal confluence is preserved
4 Hilar stricture, with involvement of confluence and loss of communication
between right and left hepatic duct
5 Involvement of aberrant right sectorial hepatic duct alone or with concomitant
stricture of the CHD
Table II. Strasberg's classification of bile duct injury
Type Criteria
A Cystic duct leaks or leaks from small ducts in the liver bed
B Occlusion of a part of the biliary tree, almost invariably the aberrant right
hepatic ducts
C Transection without ligation of the aberrant right hepatic ducts
D Lateral injuries to major bile ducts
E Subdivided as per Bismuth's classification into E1 to E5
Table III. The Amsterdam Academic Medical Center's classification of bile duct injury
Type Criteria
A Cystic duct leaks or leakage from aberrant or peripheral hepatic radicles
B Major bile duct leaks with or without concomitant biliary strictures
C Bile duct strictures without bile leakage
D Complete transection of the duct with or without excision of some portion of the
biliary tree
21
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