Surg Endosc and Other Interventional Techniques

DOI 10.1007/s00464-013-3081-6

ATOM, the all-inclusive, nominal EAES classification of bile duct

injuries during cholecystectomy
A. Fingerhut • C. Dziri • O. J. Garden •

D. Gouma • B. Millat • E. Neugebauer •

A. Paganini • E. Targarona

Received: 17 June 2013 / Accepted: 24 June 2013

Ó Springer Science+Business Media New York 2013

Abstract classification, combining all existing classification items,

Background Several studies seem to indicate at least a taking into account the changing pattern of BDI.
2-fold increase in bile duct injuries (BDI) since the Methods Extensive bibliographic research, analysis of
inception of laparoscopic cholecystectomy. Moreover, each category within the individual classifications com-
injuries seem to be more proximal, seem to be revealed bined into one uniform classification.
earlier, are expressed by leaks more often than by stric- Results Fifteen classifications were retained. All items
tures, are repaired more frequently by nonspecialists (either were integrated into the European Association for Endo-
during the index operation or soon after), and appear to be scopic Surgery (EAES) classification, using semantic
more often associated with loss of substance and ischemia. connotations, grouped in three easy-to-remember catego-
The plethora of prior classifications probably attests to the ries, A (for anatomy), To (for time of), M (for mechanism):
evolving clinical spectrum, the mounting wealth of ever- (1) the anatomic characteristics of the injury: NMBD for
increasing diagnostic methods, and an acknowledgment of non-main bile duct or MBD for main bile duct (followed by
insufficiencies or lack of data in earlier classification a number 1–6, corresponding to the anatomic level on the
reports. Previous attempts at uniformity remain incom- MBD), followed by Oc (for occlusion) or D (division), P
plete. The purpose of this study was to devise a nominal (partial) or C (complete), LS (loss of substance), VBI
(vasculobiliary injury in general), and whenever known,
the vessel; (2) time of detection: Ei (early intraoperative),
Electronic supplementary material The online version of this Ep (early postoperative) or L (late); and (3) mechanism of
article (doi:10.1007/s00464-013-3081-6) contains supplementary injury: Me (mechanical) or ED (energy-driven).
material, which is available to authorized users.

A. Fingerhut (&) D. Gouma

First Department of Surgery, Hippokration Hospital, University Surgical Department, Academic Medical Center, Amsterdam,
of Athens Medical School, Athens, Greece The Netherlands
e-mail: [email protected] e-mail: [email protected]

A. Fingerhut B. Millat
Section for Surgical Research, Department of Surgery, Medical Surgical Department, Hôpital St Eloi, University of Montpellier,
University of Graz, Graz, Austria Montpellier, France
e-mail: [email protected]
C. Dziri
Surgical Department B, Charles Nicolle University Hospital, E. Neugebauer
Tunis, Tunisia IFOM FOM–Institut für Forschung in der Operativen Medizin
e-mail: [email protected] Lehrstuhl für Chirurgische Forschung Private Universität
Witten/Herdecke, 51109 Cologne, Germany
O. J. Garden e-mail: [email protected]
Clinical Surgery, Royal Infirmary, University of Edinburgh,
Edinburgh EH3 9YW, UK
e-mail: [email protected]

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Conclusions The EAES composite, all-inclusive, nominal during the 19th EAES meeting in Turin, Italy, in June 2011
classification ATOM (anatomic, time of detection, mech- [26], several members of the consensus conference and
anism) should allow combination of all information on three outside European experts in the field of biliary sur-
BDI, irrespective of the original classification used, and gery (OJG, DG, and BM) thought that it would be timely to
thus facilitate epidemiologic and comparative studies; devise a new uniform classification with two goals: first, to
indicate simple, appropriate preventive measures; and take into account the changing pattern of injuries incurred
better guide therapeutic indications for iatrogenic BDI since the introduction of laparoscopic cholecystectomy;
occurring during cholecystectomy. and second, to combine all the existing items in the most
widely used classifications to date into one all-inclusive,
Keywords Bile duct injury
Biliary injuries
universally accepted classification [15]. This would allow
Cholecystectomy
Classification
Laparoscopic collection of data useful for further epidemiological and
cholecystectomy
Laparoscopy
Vasculobiliary injury comparative studies as a comprehensive classification that
collates all types of injury, whether culled independently
by endoscopists, radiologists, or surgeons, integrated into a
Current data seem to point to at least a 2-fold increase in user-friendly, anonymous, electronic registry. This may
the iatrogenic bile duct injury (BDI) rate during laparo- lead to a more precise determination of the true incidence
scopic cholecystectomy compared with that reported for of BDI incurred during laparoscopic cholecystectomy and
open cholecystectomy [1–4]. Likewise, the pattern of such thus to the creation of preventive measures.
injuries has changed: BDI sustained during laparoscopic
surgery appear to be more proximal [5, 6]; revealed earlier
(by leaks, collections, or biloma more often than by stric- Methods
tures [7, 8]; associated more often with loss of substance
[9, 10] and ischemia, whether related to concomitant vas- An extensive bibliographic research was performed by que-
cular injuries [11, 12] or to energy-driven lesions of the rying PubMed, Medline, Embase, and Ovid SP (version
bile duct [13–15]; and repaired more frequently by non- OvidSP_UI03.02.04.102; Ovid Technologies, New York,
specialists during the index operation, or soon afterward. NY, USA) databases from 1990 to 2013 with MeSH terms as
Numerous BDI classifications have been devised since follows: classification, biliary injuries, bile duct injury, vas-
the still widely used Bismuth classification [13, 15–24] culobiliary injury, laparoscopic cholecystectomy, laparos-
(Online Supplementary Material). The cornucopia of copy, cholecystectomy, with the following Boolean operators:
classifications probably attests to the recognition of the classification AND laparoscopic cholecystectomy AND
evolving clinical spectrum, the mounting wealth of ever- cholecystectomy AND biliary injury AND bile duct injury
increasing diagnostic methods as much as acknowledgment AND biliovascular injury. Additional articles were searched
of insufficient descriptions or variations of injury, and in by manual identification of references contained in the key
particular variation in the very definition of BDI in previ- articles. There were no language restrictions on our initial
ous reports [11, 25]. Efforts at uniformization or combi- search, but only classifications either published in English or
nation of existing classifications have been made [15, 16] translated into English by the authors were included and
but remain incomplete. However, one of the major draw- analyzed. The search was limited to classifications involving
backs is that most of these classifications attach specific BDI related to cholecystectomy or bile duct surgery for benign
BDI (occlusion, division, partial, or complete) with a disease. We eliminated reports of BDI that resulted from
specific anatomical level, while in fact these injuries can trauma, malignant disease, liver, pancreatic or gastroduodenal
occur almost anywhere and in a variety of ways. ulcer disease, or surgery thereof.
In view of these inconsistencies and variations, and at All authors analyzed the strengths and weaknesses of
the occasion of the European Association for Endoscopic each classification and then through a Delphi process
Surgery (EAES) consensus conference on iatrogenic BDI composed an all-inclusive nominal EAES classification.
An anonymous electronic database was set up on the EAES
Web site (http://www.eaes.eu).
A. Paganini
Divisione de II Clinica Chirurgica, Dipartemento de Rome,
Rome, Italy Results
e-mail: [email protected]
Classification in the literature
E. Targarona
Surgical Department, Sant Pau University Hospital,
Barcelona, Spain Of 67 articles found with the above-mentioned search
e-mail: [email protected] methodology, 18 articles contained classifications and/or

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modifications thereof [1, 8, 9, 11, 13, 15–17, 19–21, 23, 24, occluded (O) (ligation, clip, sealed) or divided (D) [11, 24]
27, 28], along with two English translations [29, 30]. All and leaked. In both of these, the lowercase letter ‘‘c’’ is
related to BDI occurring during cholecystectomy. The total added to stand for complete interruption (ligation, clip,
number of classifications retained for analysis was 13; two sealing, or division), while a partial interruption (ligation,
additional items were derived from partial classifications clip, sealing, or division) is labeled ‘‘p,’’ followed by the
[6, 22]. The Appendix provides more information about the percentage of the circumference involved whenever this
classification systems. detail is known, whether there was a loss of substance
The classifications [1, 8, 9, 11, 13, 15–17, 19–21, 23, 24, between two divisions, irrespective of whether one or both
27–30] have strong positive points but also weaknesses of the extremities was occluded or divided (LS; the length
(Table 1). in centimeters, whenever known, is indicated in parentheses).
Concomitant vasculobiliary injury (VBI) is defined as an
EAES all-inclusive classification injury to both a bile duct and a nearby vessel [12]. Our
definition also includes vascular injury that occurs alone in
Combining all the items found in these 15 classifications the index operation but results in injury, such as septic
[1, 8, 9, 11, 13, 15–17, 19–21, 23, 24, 27–30], a composite complications, stricture, or liver atrophy. The BDI may be
classification was devised: the EAES all-inclusive classi- caused by operative trauma, may be ischemic in origin, or
fication, which divided the injuries into three easy-to- may be both; and it may or may not be accompanied by
remember overall categories known by the mnemonic various degrees of hepatic ischemia. When the injured
ATOM (anatomic, time of detection, mechanism). Each is (whether repaired, sealed off, or ligated) vessel is known,
discussed in turn. the following abbreviations can be added to VBI and
included in the detailed electronic analysis: RHA, right
Anatomic characteristics of the injury hepatic artery injury, which is the most often involved [11];
LHA, left hepatic artery; CHA, common hepatic artery;
This includes the anatomic level on the biliary tree of the and PV, portal vein.
initial injury and concomitant vasculobiliary injury.
The biliary tree is divided into the main and nonmain Time of detection
biliary ducts. The main biliary duct (MBD in the EAES
classification) (including the common biliary, the common The time of detection is classified as early (E) or late (L).
hepatic, and the right and left hepatic ducts) derived from Within the early detection group, a separation is made
the Bismuth, Strasberg, Neuhaus, Connor class E, McMa- between the intraoperative (Ei) and the immediate post-
hon, and Lau classifications [6, 8, 9, 15, 18, 19, 24, 29]. operative detection groups (Ep) because the latter may be
Only the anatomic localization is given, not the associated accompanied by inflammation and/or sepsis [31], whereas
lesions indicated in these cited classifications. The types the former is usually discovered by the presence of bile in
are as follows: type 1, low main BDI C 2 cm distal to the operative field or at intraoperative cholangiogram [6, 7,
inferior border of superior hepatic confluence; type 2, 15, 18]. Pulitano et al. [32] defined the early postoperative
middle main BDI \ 2 cm distal to inferior border of period as fewer than 7 days because of the therapeutic
superior hepatic confluence; type 3, high main BDI implications of concomitant arterial injury. This period
involving the superior hepatic confluence but the left–right should allow detection of most bile leaks as well. In
communication is preserved, usually on the roof; type 4, addition, the onset of liver abscess several days or weeks
high main BDI involving the superior hepatic confluence after, or discovery of hepatic atrophy [11, 32] several years
but left–right communication is interrupted, including the after cholecystectomy would be an indication of a lesion to
E6 injury of Connor and Garden [6]; type 5, left or right one of the main hepatic ducts—for instance, a Strasberg
hepatic duct injuries without injury to the superior con- type B or type E IV lesion [24], or a vascular lesion
fluence; and type 6, isolated segmental hepatic duct injury (Stewart class D) [11].
(right anterior or posterior sectorial; Li type 1) [22].
The non-main biliary duct (NMBD in the EAES clas- Mechanism of injury
sification) includes the cystic aberrant and accessory
(hepatic bed, subhepatic, or Luschka) ducts, corresponding The mechanism of injury may be classified as mechanical
to Strasberg types A and C, Neuhaus A, Lau 1, Amsterdam (Me) (e.g., scissors, Dormia basket stone extraction) or
type A, and Li type 2 [9, 15, 19, 22, 24, 28, 29]. The type as energy driven (ED) (e.g., cautery or ultrasonic) injury.
well as the circumferential and longitudinal extent of injury The EAES classification label for BDI thus includes a
depends on whether the injured bile duct was initially series of acronyms: MBD for main bile duct (followed by a

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Table 1 Bile duct injury classifications in the literature
Study Anatomical characteristic Time of detection Mechanism of injury
MBD/NMBD Level of injury Type and extent of injury of bile ducts VBI Ei Ep L Me/ED
Oc D (leak) LS
c p c p

Bismuth [13, 18, 19] ? ? d d d d - - - - ? i

Strasberg et al. [24] ? ? a d ? ? a a a a ? ±I, k
McMahon et al. [8] ? a a - ? ? a - a a ? a
AMA [19, 28] ? a e e d d a - a a ? -
Neuhaus et al. [9, 29] ? ? ? ? d ? f, g a ± - ? j
Csendes et al. [20] - b - - d d ? ?h - - ? k
Stewart et al. [11] - b d d ? ? ? ?h - - k ?
Hanover [16, 27] ? ? ? ? ? ? g ? a a ? ±j
Lau and Lai [15] ? ? d d ? ? ? ?h ? ? - -
Siewert et al. [10, 30] ? ±a, b d d ? ? g a - ? ? -
Cannon et al. [1] ? c - - - - - ?h - - - -
Kapoor [21] ? b ? ? ? ? ? ?h j - -
Sandha et al. [23] a b - - - - - - - - - -
EAES ? ? ? ? ? ? ? ? ? ? ? ?
a discussed but no clear explanation of how to include it in the classification; b no clear discriminator of level of injury; c Hanover classification for level of injury, but only for one category (III)
of lesions (but also refers to Bismuth); d no distinction between partial (P) and complete (C) or this distinction is not indicted for all types or localizations; e no distinction between division left
open (leak) and occlusion; f distinguishes between longitudinal partial lesions less than or more than 5 mm; g not clear what is meant by ‘‘defect’’ or ‘‘structural defect’’ (loss of substance?);
h no indication of which vessel; i energy driven injury recognized but not indicated in the classification; j injury by clip recognized but no differentiation between mechanical and energy-driven
injury; k recognizes mechanical and electric injury but no distinction between the 2 in the classification; l distinguishes between division left open (bile leak) and occlusion
Classification is according to whether and how the anatomical characteristics, time of detection, and mechanism of injury were included in the classification. The EAES classification includes:
MBD main biliary duct or NMBD non-main biliary duct, a number (1–6, corresponding to the anatomic level according to Bismuth except for 5) followed by the letters C (complete) or P
(partial). Oc occlusion; D division; LS (cm) loss of substance (length); VBI vascular biliary injury; RHA, LHA, CHA, PV, or MV, for vascular biliary injury to the right hepatic artery, left hepatic
artery, common hepatic artery, portal vein, and marginal vessels, respectively, if the injured vessel is identified; Ei, Ep, or L early intraoperative, early postoperative, or late for time of detection;
and Me mechanical or ED energy driven for the mechanism of injury
EAES European Association for Endoscopic Surgery, ? yes, - not included or discussed
Surg Endosc
Surg Endosc

Table 2 EAES classification matrix for bile duct injuries

Anatomical characteristics Time of detection Mechanism

Type and extent of injury Vasculobiliary
injury
occlusion division (yes=VBI+)
and name of Ei
Anatomic
injured vessel (de visu, bile Ep L Me ED
level
(RHA, LHA, leak, IOC)
C P* C P* LS**
CHA,
PV, MV);
(no = VBI-)
MBD
1
2
3
4
5
6
NMBD

For each injury, the surgeon fills in the following matrix: (1) single injury (yes/no); (2) multiple injuries (yes/no). Then one matrix is filled in for
each injury, as appropriate. For example, an injury made by an energy-driven (ultrasonic) dissector involving the superior biliary confluence with
interruption of the right and left hepatic ducts, detected (intraoperatively) during the operation by the presence of bile would be classed as MBD 4
C VBI Ei, ED. The Connor Garden E6 injury is in fact a type 4 with LS: MBD 4 LS
EAES European Association for Endoscopic Surgery, MBD main biliary duct, NMBD nonmain biliary duct (Luschka duct, aberrant duct,
accessory duct), level 1 C 2 cm from lower border of superior biliary confluent, level 2 \ 2 cm from lower border of superior biliary confluent,
level 3 involves the superior biliary confluent but communication right left is preserved, level 4 involves superior biliary confluent but
communication right left is interrupted, level 5a right or left hepatic duct, level 5b right sectorial duct but bile duct still in continuity, C complete,
P partial, LS loss of substance, Me mechanical, ED energy driven, VBI vasculobiliary involvement, RHA right hepatic artery, LHA left hepatic
artery, CHA common hepatic artery, PV portal vein, MV marginal vessels, Ei early intraoperative, Ep early postoperative, L late, OC intra-
operative cholangiogram
a
Indicate percentage of circumference, if known
b
Indicate length, if known

number 1–6, corresponding to the anatomic level on the therapy, and allow comparison of management and out-
main bile duct), NMBD for nonmain bile duct, followed by comes between different series.
the relevant acronyms (Table 2): O or D, each with the There are several ways of setting up a classification:
suffix c or p (%), LS (cm), VBI (RHA, LHA, CHA, PV, either letters or numbers are used in an ordinal (succession
marginal vessel [MV]), Ei, Ep, or L, and Me or ED. If for of letters or numbers) or even a cardinal fashion, or letters
some reason a parameter is unknown, the suffix ‘‘?’’ is are used in a nominal fashion to signify the word they
added. imply (i.e., semantics). Most of the classifications analyzed
herein follow some logical order for some items, but not
for the entire list. None of the classifications analyzed
Discussion herein was scaled to note the progression in an ordinate
fashion. Only a few classification schemes [18, 21, 27],
The composite EAES all-inclusive classification enlaces all including ours, use letters (usually the first letter of the
possible BDI described in the literature into one global corresponding word) and are based on the meaning or
classification, which we consider a possible universally semantics behind the letters, thus making it easer to
accepted classification because of its exhaustive character. remember, but the words used in the previous classifica-
By dividing BDI into three simple categories (anatomic, tions varied in meaning and in language (Appendix).
time of detection, mechanism), abbreviated ATOM, we
tried to make it easy to remember. Advantages of the EAES classification
Classifications are useful for several reasons. They can
provide an anatomic picture of the lesion, help classify the There are several advantages to the EAES classification.
lesions according to severity of prognosis or to complexity Because the EAES classification contains all the possible
[15], provide insight to the mechanisms responsible and items found in the 15 other classifications, all reports of
thus lead to preventive measures, serve as guidelines for BDI can be integrated into the EAES matrix and then used

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Table 3 EAES classification matrix for moment of occurrence of There are two types of cystic duct leaks. First, either the
BDI cystic duct was identified, clipped, ligated, or eventually
Item Check if sealed with an ultrasonic or bipolar device but then leaked
present because the clip or ligation was insufficiently placed (i.e.,
not including the entire diameter); because the clip or
Before identification of cystic triangle elements
sealing was ineffective (failed), or because the ligation or
During identification (dissection) of cystic triangle
elements the clip fell off (Hanover A1 [16, 27], Neuhaus A1 [9, 29],
After identification of cystic triangle elements Strasberg type A [24], Siewert type 1) [10, 30]; or because
(clipping, energy-driven or ligation of cystic artery the sealing was insufficient. This is not, strictly speaking, a
or duct, opening of the cystic duct for IOC); BDI, as injury is defined as harm or damage that is done or
misinterpretation of above mentioned structures) sustained, but rather is a biliary complication [6]. More-
Before cholecystectomy over, it can be a sign of increased ductal pressure, due, for
During cholecystectomy example, to a retained stone, with a rate as high as 12.3 %
After cholecystectomy in one series [33]. Likewise, leakage from the cystic duct at
During dissection or maneuvers for stone extraction the Hartmann pouch after subtotal cholecystectomy cannot
from main bile duct via cystic duct
be considered a BDI. Last, the Stewart class I (cholangi-
During dissection or maneuvers for stone extraction
ogram cystic duct incision that extends into the common
from main bile duct via common bile
bile duct [CBD]) [11] and Csendes type 2 (lesions of the
During IOC (opening the cystic duct or what is
thought to be so), introduction of catheter or cystic–choledochal junction due to excessive traction,
instrument for IOC) section of the cystic duct very close or at the junction with
During other maneuvers (hepaticoenterostomy) the CBD [20], or a thermal injury to the cystic–choledochal
After IOC (withdrawal of catheter or instrument) junction, even when transmitted by metallic clips placed on
During mechanical or energy-driven injury for the cystic ducts are CBD [MBD] injuries) are not, strictly
elective hemostasis or ligation speaking, cystic duct injuries.
Mechanical or energy-driven injury for unexpected The second, more correctly called a BDI, is when the
bleeding cystic duct is opened unwillingly (e.g., because of obscure
From EAES (http://www.eaes.eu) anatomy) because of an impacted stone or because of
EAES European Association for Endoscopic Surgery, BDI bile duct misidentification, but left untreated.
injury, IOC intraoperative cholangiogram There are at least two arguments in favor of including
cystic duct injuries in our classification. First is the classic
Davidoff injury [34], where the cystic is ligated, clipped, or
for epidemiology studies and comparison between pub- sealed proximally, near the gallbladder, but where the
lished series (Table 3). distal ligation, clip, or seal is placed on the CBD. The distal
We distinguished between main biliary duct injuries hepatic duct stump between these two sites is left open and
(MBD) and non-main biliary duct injuries (NMBD), i.e., bile flows freely into the peritoneal cavity. This lesion
the cystic duct, liver bed (including Luschka), and aberrant would be classed as both MBD and NMBD, Oc and D, and
ducts. NMBD injuries were individualized in 7 of the 13 LS. Second is because it would include both leaks due to a
full classifications (Strasberg type A and C, Neuhaus A, clip placed on the cystic duct, at the junction with the CBD,
Hanover A, Siewert type 1, Keulemans, Bergman A, that slides off and leaves what then appears to be a lateral
Cannon 1, Lau) [1, 9, 10, 15, 16, 19, 24, 28–30], but not the defect in the CBD (Csendes type II [20], Strasberg type A
6 others [8, 11, 13, 16, 17, 20, 21, 23] (Table 1). Unlike [24]) and energy-driven ischemic secondary openings—for
several classifications, we made a distinction between instance, enhanced by a metallic clip placed on the cystic
segmental hepatic ducts (MBD type 5 and the other NMBD duct.
duct injuries)—again, because of the therapeutic conse- The importance of the type of interruption (occlusion or
quences that they imply [15, 21, 22]. From a semantic point division) and degree or extent of circumferential and lon-
of view, this system (MBD and NMBD) was preferred to gitudinal interruption derives from the differences between
small [15, 20], major, and minor, as implied by the occlusion (closure of the bile duct by ligation or clip) and
Amsterdam Academic Medical Center [19, 28] and Stras- division (solution of continuity), with the latter either
berg et al. [24] classifications, which may be confused with occluded or left open. Both occlusions and divisions can be
connotations of severity, as implied in the McMahon complete (360°) or partial (less than 360°). Partial occlu-
classification [8]; or peripheral [9, 18, 27, 29] and central sion can be clinically silent but can result in stricture [35],
[10, 30], or significant and insignificant, used by Kapoor or if ischemia occurs, secondary necrosis and leak. Com-
[21]. plete occlusion of the MBD creates upstream retention with

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early (jaundice, sepsis) or late (atrophy) symptoms. Com- already been done (artery ligation, opening of the bile duct)
plete occlusion of NMBD (Strasberg type B [24], Csendes and the moment when the BDI is detected—for example,
D [20]), depending on the extent of territory involved, can during the index operation, the immediate postoperative
be clinically silent (slight perturbation of liver function period (often with sepsis), or late (stricture). Although one
tests) or symptomatic. The distinction between occlusions, recent report found that 17 of 19 (89.4 %) BDI were dis-
either complete (Oc) or partial (O), with division (D) (also covered intraoperatively in a series of 10,123 cholecys-
either Dc or Dp) leading to a leak is important to consider tectomies [38], only up to one third of BDI were usually
[9, 24, 29] because the diagnosis and treatment are often recognized during the operation [6, 7, 15, 18]. As pointed
quite different [15]. Leaks are rarely diagnosed during the out by others [24, 38–40], the value of intraoperative
operation [31]; more often they result in early postopera- cholangiogram is its ability to demonstrate the injury
tive bile collections and sometimes in bile peritonitis. intraoperatively, leading to early discovery and ideally
Several authors [8, 9, 15, 19, 20, 24, 28–30] have distin- early repair, before inflammation and infection set in.
guished partial (tangential) from complete division, but, Occlusion of a part of the biliary tree (Strasberg type B
with the exception of McMahon et al. [8], without any lesions [24], not individualized by either the McMahon
precision as to the circumference involved. Although most et al. [8] or Bismuth [13, 18, 19] classifications) are rarely
incomplete injuries of the main biliary tract (MBT) are discovered early. These injuries may remain asymptomatic
indeed lateral in the anatomic sense of the word—and are or present 10 or more years after the initial insult with pain
depicted as a such [9, 11, 20, 24, 29]—partial might be a or cholangitis [41] or liver atrophy [6].
better term because some injuries can be anterior, posterior, Vascular injuries are essential to consider for several
or more rarely median, or any combination thereof. This is reasons: when vascular injuries occur during the operation,
captured by our classification. they are a potential source of blood loss, and blind
When a loss of substance occurs, this is indicated as LS. hemostasis is often the cause of BDI; hemostasis of a ter-
The term loss of substance was preferred to the terms minal major biliary tract vessel means that downstream
defect [16, 27], structural defect [9, 11, 29, 30], excision ischemia will ensue; vascular injuries can occur by
[19, 28, 36], or tissue loss [15]. In the so-called classical mechanical division (scissors or electronic scalpel) or by
Davidoff injury [34], the CBD is mistaken for the cystic secondary thrombosis, either through energy-driven prop-
duct and is injured in two spots: when the surgeon secures agation (diffusion) or accidental coagulation; the marginal
what is believed to be distal portion of the cystic duct, and arteries are cut at the same time as the duct; and con-
at the common hepatic duct that is believed to be the comitant vascular and ductal injury (even when the latter is
proximal segment of the cystic duct leading to the gall- repaired) increases the risk of long-term bile duct stricture
bladder. The E6 type injury of Connor and Garden [6] [14] and liver atrophy [32], and perhaps equally stricture
consists of complete excision of the extrahepatic biliary and restricture of a hepatoenterostomy performed too close
duct, including the confluence, and would be a combination to the initial injury [37].
(addition) of EAES types 3 and 4 with LS. Whenever We chose not to indicate whether the BDI was the
known, the length of the loss of substance is indicated consequence of an opening in the main bile duct with the
because the length of the loss of substance and the length of intention of accomplishing or not accomplishing an action,
stricture when this complication occurs both have their such as inserting a catheter; removing a stone, parasite, or
importance for surgical treatment [19, 20, 24, 28], balloon foreign body; or preparing an anastomosis. We had several
dilatation, or stenting [37]. To the contrary of several reasons for this. First, we did not want to use the word
classifications, strictures were not included in our classifi- intentional, as its definition is not universal. Second, the
cation because stricture is the result of an injury, not the term has a medicolegal connotation. Finally, most often the
injury itself. opening (e.g., choledochotomy [11, 24]) is recognized and
The distinction between partial and complete division is closed, ideally or over a T tube. We recognize, however,
(with E6 [6] or without separation [B4] [13] or loss of that the closure of any opening in the bile duct can leak,
substance) has its importance in repair. Partial BDI is reopen, and/or evolve to a later complication such as
easier to treat endoscopically or even surgically when bile stricture. The term purposeful might be more appropriate.
duct continuity is respected [15]. All intraoperative BDI, especially when considered
We also included the timing of BDI detection intraop- minor, whenever repaired immediately by the same sur-
eratively, either by a bile leak or cholangiography, or the geon, should be reported as injuries. Injuries treated
early consequences thereof, such as a biloma, abscess, or endoscopically, injuries that result in intra-abdominal bile
biliary peritonitis, or invariably late, resulting in stricture or collection only, or injuries in strictures not seen or treated
hepatic atrophy. The importance of this categorization is by surgeons (e.g., drained and/or treated by interventional
because management is different according to what has radiologists) may be underreported in surgical series but

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may be more prevalent in endoscopic or interventional all injuries systematically in the operative note, is to vali-
radiology. This is notably the case for NMBD injuries (e.g., date this classification by a prospectively gathered cohort
Strasberg type A, McMahon minor, Neuhaus 1) [8, 9, 25, and to set up a registry. The EAES has devoted a specific
29]. Combining surgical classifications with endoscopic part of its Web site to this endeavor and provides classi-
classifications, such as the EAES endeavor, should lead to fication forms that can be downloaded (Table 2) (http://
a more accurate account of the true incidence of BDI. www.eaes.org/). Ideally, these data, as well as a specific
table related to detection, patient-related data, and infor-
Study limitations mation about the type of repair, should be collected in a
prospective European registry that ensures patient and
Although we have endeavored to make this classification surgeon anonymity.
comprehensive, it has several shortcomings. We recognize This all-inclusive, semantics-based classification should
that this classification is complex. However, when dealing enhance further research by helping determine the true
with BDI, surgeons familiar with this type of surgery incidence of BDI during laparoscopic cholecystectomy. It
should not be in any hurry to categorize these lesions. will help us understand the underlying mechanisms so
Rather, they should strive to be complete and precise. All preventive and adapted therapeutic measures may be
reports using one or another of the existing classifications proposed.
ought to be entered into a matrix (Table 2) that can then be
used for universal reporting and comparisons. Disclosures A. Fingerhut, C. Dziri, O. J. Garden, D. Gouma, B.
Millat, E. Neugebauer, A. Paganini, and E. Targarona have no con-
Our classification does not provide an exact progressive flicts of interest or financial ties to disclose.
picture of the intensity or severity of the lesion. Although
there seems to be a progression in severity when one goes
from Bismuth 1 to 4 [13, 18, 19], from partial to complete
transection, or from closed to open duct leaks, the same is
not true for the other grades of our classification or for the Appendix: legend to Table 1
other classifications. Moreover, Bismuth 6 [13] is not
always more severe than B5 [18, 19] (or E6 of Connor and Bismuth’s classification was originally proposed to catalog
Garden [6]). postoperative strictures and to stratify their treatment.
As in other classification systems, there may be some Therefore, the emphasis was placed on the length of
overlap. For instance, the discovery of liver atrophy [11, healthy distal bile duct mucosa proximal to the injury [18,
32] several years after cholecystectomy could attest to the 19]. A level 6 was added in to the original 5 levels of
presence of a lesion in one of the main hepatic ducts and/or stricture in 2001 [13] to indicate isolated right duct or right
a vascular lesion. branch strictures. Of note, the level of stricture (lower
We did not distinguish between injuries experienced limit) does not always correspond to the level of injury [13]
during the index cholecystectomy or at secondary repair, as because of potential initial ischemic or thermal damage as
suggested by Connor and Garden [6] and Stewart et al. well as the shortening that often accompanies upstream
[11]. The lesions are basically the same but admittedly dilatation of the duct. This is why the initial site of the
probably more destructive, with additional vascular insult; injury is indicated to define the injury level in the EAES
detection and repair are far more complex. classification. However, it is acknowledged that the length
The exact moment during the operation of when the BDI of stricture has direct therapeutic implications [37], and
took place was not included. We do, however, believe that this parameter is found in the length of ‘‘loss of substance.’’
knowing the moment the BDI occurs means it can be The Bismuth classification does not account for acute
prevented—or at least discovered early and repaired, again injuries (e.g., transection) or leaks; there is no mention of
highlighting the value of intraoperative investigations, vasculobiliary involvement.
notably intraoperative cholangiogram [39, 40]. The matrix The classification of Strasberg et al. [24] was specifi-
in Table 3 aims to classify the moment when the BDI cally devised for laparoscopic injuries. It is comprehensive
occurs. in that it includes a wide spectrum of injuries, including
intra- and extrahepatic injuries. Strasberg et al. distin-
guished between occlusions (types B and E), occlusions
Conclusions leading to biliary obstruction, and divisions without
occlusion (types A, C, and D), leading to leaks and bilo-
All surgeons practicing bile duct surgery ought to report all mas. They also classified isolated occlusion of the right
BDI, even those that they consider part of the operation or hepatic duct (missing from the Bismuth classification).
those repaired immediately. A second step, after reporting Although the authors made the distinction between

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complete (type C) and partial division (type D), partial circumference and thus be a major injury. Moreover,
occlusion is missing. The classification insists on mecha- although the distinction had certain therapeutic implica-
nisms and technical errors. It also includes the location tions at the time the classification was derived, today, a 30
(integrating the Bismuth classification). However, partial % to 35 % circumference injury might still be quite easily
division can be located on the CBD, common hepatic duct repaired surgically or by stent insertion [31], whereas the
(CHD), left hepatic duct, or right hepatic duct (RHD), and treatment options are not the same when the injury involves
this anatomic distinction cannot be categorized. Also, 90–99 % of the circumference. However, in this classifi-
included in type A injuries are cystic duct leaks that occur cation, both types of injury are classed in the same ‘‘major’’
as a result of physical injury as well as insecure clips or group. These authors made no distinction between division
ligatures, leading to the question of whether this latter (laceration and transection) and occlusion, and they did not
mechanism truly represents a bile duct injury or, as stated mention longitudinal loss of substance or vasculobiliary
by Connor and Garden [6], a biliary complication. Of note, involvement. Similar to Strasberg et al. [24], and McMa-
type B and C injuries occur mainly when an aberrant right hon et al. [8] included the Bismuth classification to des-
duct is mistaken for the cystic duct when the latter runs ignate the length of proximal healthy bile duct. However,
directly into the RHD (rather than the CHD), an anomaly they describe a class 0, which is not mentioned in any other
that involves between 2 % [42] and 28 % [43] of the publication on the topic and which does indicate how to
population. Types A, B, and C can occur in almost any integrate ‘‘major/minor’’ or the anatomic level into the two-
location along the biliary tree, not only in an aberrant RHD. category classification other than by a full description.
Strasberg et al. suggested that it would be interesting to The Amsterdam Academic Medical Center classification
subclassify injury according to whether there was a loss of derives from two publications [17, 28]. Most of the diag-
substance and the length of the loss of substance; according noses were made postoperatively, through endoscopic and/
to injury with devascularization but without division; and or percutaneous transhepatic cholangiography. Although
according to concomitant injury to the right hepatic artery mentioned and discussed, the classification itself does not
(RHA) (in types E1 and E2). However, they did not include indicate the location of the injury, except for A (cystic duct
these injury profiles in their classification. Theoretically, and aberrant or peripheral hepatic radicals); B I (main
types B, C, and D involve the main bile duct but do not CBD); and B II (aberrant segmental extrahepatic branches).
indicate the level of injury. The varieties e, d, and f in type It is not clear what the authors mean by ‘‘minor’’ and
E lesions are in fact redundant with types B and C. Last, ‘‘major’’—whether this represents ‘‘not severe’’ and
type E categorizes occlusion but not division of the bile ‘‘severe,’’ injury to the NMBD and MBD, or partial
ducts above the superior confluence. Adequate and com- (B) versus complete (D) divisions. Bile leaks from the
plete use of this classification should therefore include a cystic duct, aberrant or peripheral hepatic radicals, and
letter A to D for the type plus, an E number, for the minor bile duct lesions are lumped together in type A. Type
location, which is rarely seen in the literature. All these D injuries include complete transection, but nothing in the
variations were included in our classification. classification allows us to determine whether there has
McMahon et al. [8] divided lesions according the extent been a loss of substance. The classification does not pro-
of damage to the main bile duct, including laceration, vide insight into the mechanism of injury. There is no
transection, or excision, or, later, as stricture, leading to a distinction between complete transection with (the bile
simple two-class separation, minor and major. Minor ducts will dilate) or without (the bile duct will leak)
includes\25 % of circumference of the CBD, laceration of occlusion (ligature, clip). Last, there is no mention of
the cystic CBD junction, or both. Major includes[25 % of vasculobiliary involvement.
circumference, going all the way to full transection, and The classification of Neuhaus et al. [9] was originally
involves the common bile or hepatic ducts. This classifi- published in German; an English translation can be found
cation has several negative aspects. For example, minor in Schmidt et al. [29]. This classification individualizes the
injuries are described for the CBD only, while major injury nonmain BDI (type A), distinguishing between cystic duct
involves the CBD and CHD, without mention of injury (A1) and hepatic bed leaks (A2). However, it does not
including or above the superior confluence. Another neg- separate the physical cystic duct injuries from leaks due to
ative aspect is that the cutoff of 25 % is arbitrary: minor slipped clips or ligatures. It incorporates vascular injuries,
injury can encompass a variety of injuries (Strasberg types but these are not integrated into the figures, and there is no
A, B, C, and D) and ultimately can result in stricture (a indication as to how to list them. The length of injury (type
major injury). Both a lateral laceration of less than 25 % of C) as well as loss of substance (‘‘structural defect’’) are
the circumference and the laceration of the cystic CBD included. However, the 5-mm cutoff value for length of
junction are in the same category, minor, whereas the same injury is arbitrary, with no explanation of why this was
type of latter injury can involve more than 25 % of the chosen. The level of injury is not indicated for acute

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injuries, only for stenosis. The word stenosis is used to Of note, types I and II are identical to classes I and II, but
designate stricture, which might mean any narrowing, not types III and IV are different from classes III and IV, which
necessarily one that is the result of a BDI. Last, the extent only adds to the confusion.
of circumferential damage is binominal (partial and com- The Hanover classification [16, 27] has tried to combine
plete division only, without any quantification). several items included in other classifications and comes
The classification of Csendes et al. [20], which is based close to the goal of being all-inclusive, but some infor-
on the analysis of three varied circumstances of recruitment mation is still missing. In particular, this classification does
(retrospective multicentric, prospective monocentric, and not distinguish between intraoperative and postoperative
referrals) as well as etiologic and anatomic considerations, detection of the injury, or the mechanism of injury (except
is restrictive in that there is no indication of the anatomical for the clip mechanism, type B). The authors used the term
level and it does not include injury above the superior stenosis to designate an occluded duct; this might lead to
confluence. Thus, it is difficult to distinguish between confusion with stricture. Again, the 5-mm length of loss of
partial and complete type III injuries, and there is no dis- substance was used [9, 29] without explanation of where
tinction between occlusion and division. The classification this cutoff value came from. The letters used to designate
brings forth some of the possible mechanisms, but energy- the vascular injury are based on Latin and therefore might
driven injuries are not separated from mechanical (scissors) not be integrated easily—for example, d for dextra (right),
injury, and there is no mention of vasculobiliary involve- s for sinistra (left), p for propria hepatic artery, and DHC
ment. It takes into consideration the therapeutic conse- for ductus hepatocholedochus. It is not clear what the
quences of longitudinal loss of substance (Davidoff injury) authors mean by defect in type D, particularly whether this
[20]. Moreover, it implies that injury to the RHD can represents loss of substance; if this is so, then there is no
(always) be repaired during the index operation and that clear difference between the two types of injury when they
type I and II lesions can (always) be repaired by T-tube occur above the bifurcation. The level of injury is not
insertion. indicated for acute injuries, only for ‘‘stenosis,’’ which
The classification of Way et al. [43] was originally once again is a possible source of confusion with
published in Annals of Surgery, but the Stewart et al. ‘‘stricture.’’
classification [11] is most often cited. Curiously, however, The classification of Lau et al. [5, 15], taking into
the two classifications differ somewhat because the sub- account anatomic, etiologic, and vascular problems, men-
division of class III lesions is found only in the first article tions loss of substance but does not include the short-
and is rarely used or cited. Subdivision of class III is based term cautery or ischemic injuries or the long-term septic
on the proximal extent of the injury as follows: class IIIa, consequences. It attempts to class BDI according to
remnant CHD; class IIIb, CHD transected at the bifurca- ascending order of severity as well as the date of appear-
tion; class IIIc, bifurcation excised; and class IIId, proximal ance of the complication (early and late). However, it is not
line of resection above the first bifurcation or of at least one always true that vascular injury to the right hepatic artery
of the lobar ducts. The classification is based on anatomy (type V) is more severe than type IV. Moreover, vascular
but also on the mechanism of the lesion. This classification injuries are lumped together in one class. It does not dis-
also emphasizes the role played by vascular injury, but this tinguish between sectorial and main BDI. The level of
is represented in class IV only, while this type of injury can acute injury is indicated as CBD, CHD, right/left hepatic,
occur in all four categories. The authors separate aberrant or sectorial duct.
duct from RHD injuries. The subdivision of classes IIIa and Four other simple classifications were found, one by
IIIB differentiates between common BDI without and with Siewert et al. [10] (reported in English by Weber et al.
loss of substance, but it does not describe the Davidoff [30]) and another by Cannon et al. [1], both essentially
lesion. Isolated injury (whether transection or resection) is based on economic considerations and severity; one by
described in the mechanism of injury but is not represented Sandha et al. [23] based on endoscopic findings; and one by
in the diagram. Moreover, this classification does not Kapoor [21].
provide descriptors for simple bile leaks (from the cystic The Siewert classification [10, 30] divides acute BDI
duct or the liver bed) or take into account the lesions into two anatomic categories, peripheral and central
evolving into bile duct leaks due to cautery or ischemic (probably nonmain biliary tract and main biliary tract).
injuries. It does not describe late complications, such as Siewert and colleagues [10, 30] described four types of
strictures, or identify transections at or above the bifurca- injury, noting that there was an increasing order of sever-
tion (except the RHD in class IV), and it does not cate- ity; surprisingly, late bile duct strictures, classified as type
gorize injury to the right sectorial ducts. Last, the senior II, are found between the immediate biliary fistula group
author published another classification in Wikisurgery [25] (type I) and the central lesions (types III and IV). This
in which the author used the term type as opposed to class. classification includes vascular injury, without any specific

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description for types III and IV. Derived from surgical Luschka duct lesions, and the other by Connor and Garden
series, it was used essentially to class injury before endo- [6], which added an E6 injury to the Strasberg classification
scopic-only treatment. Lesions that healed without conse- to describe complete excision of the extrahepatic confluence.
quences were apparently not recorded; this is perhaps one
of the reasons that the incidence of BDI is probably higher
than previously reported. References
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