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The American Journal of Surgery (2008) 195, 763–769

linical Surgery—International

dvantages of multidisciplinary management of bile ductnjuries occurring during cholecystectomy

ennaro Nuzzo, M.D.a,*, Felice Giuliante, M.D.a, Ivo Giovannini, M.D.a,arino Murazio, M.D.a, Fabrizio D’Acapito, M.D.a, Francesco Ardito, M.D.a,aria Vellone, M.D., Ph.D.a, Riccardo Gauzolino, M.D.a, Guido Costamagna, M.D.b,armine Di Stasi, M.D.c

Department of Surgery, Hepatobiliary Surgery Unit, Catholic University of the Sacred Heart School of Medicine, Rome,taly; bDepartment of Surgery, Digestive Endoscopy Unit, Catholic University of the Sacred Heart School of Medicine,

ome, Italy; cDepartment of Radiology, Catholic University of the Sacred Heart School of Medicine, Rome, Italy

AbstractBACKGROUND: The aim of the present study was to highlight the advantages of treatment of bile

duct injury (BDI) occurring during cholecystectomy on the basis of a multidisciplinary cooperation ofexpert surgeons, radiologists, and endoscopists.

METHODS: Sixty-six patients had major BDIs or short- or long-term failures of repair. BDI wasdiagnosed intraoperatively in 27 patients (40.9%) and postoperatively in 39 (59.1%) patients. Amongreferred patients, 30 had complications from bile leak, 15 from obstructive jaundice, and 20 fromrecurrent cholangitis. Two patients died from sepsis after delayed referral before repair was attempted.Eleven additional patients had minor BDIs with bile leak both with and without choleperitoneum.

RESULTS: Of patients with major BDI, surgical repair was performed in 41 (64.1%). Postsurgicalmorbidity rate was 15.8%, and there was no mortality. The rate of excellent or good results aftersurgical repair was 78.0% (32 of 41 patients), and this increased to 87.8% (36 of 41 patients) bycontinuing treatment with stenting in postsurgical strictures. Biliary stenting alone was performed in 23patients (35.9%), with excellent or good results in 17 (73.9%). More than 200 endoscopic andpercutaneous procedures were performed for initial assessment, treatment of sepsis, nonsurgical repair,contribution to repair, and follow-up. Patients with minor BDIs underwent various combinations ofsurgical and endoscopic or percutaneous treatments, always with good results.

CONCLUSIONS: A multidisciplinary approach was of paramount importance in many phases oftreatment of BDI: initial assessment, treatment of secondary complications, resolution of sepsis,percutaneous stenting before surgical repair, dilatation of strictures after repair, final treatment inpatients not repaired surgically, and follow-up.© 2008 Elsevier Inc. All rights reserved.

KEYWORDS:Bile duct injury;Laparoscopiccholecystectomy;Mortality;Multidisciplinaryapproach;Sepsis

isig

* Corresponding author. Tel.: �011-39 06 30154967; fax: �011-39 06058586.

E-mail address: gennaro.nuzzo@rm.unicatt.it or fgiuliante@rm.unicatt.it

tManuscript received May 26, 2006; revised manuscript May 10, 2007

002-9610/$ - see front matter © 2008 Elsevier Inc. All rights reserved.oi:10.1016/j.amjsurg.2007.05.046

Cholecystectomy is one of the most frequently performedntra-abdominal procedures. The widespread use of laparo-copic cholecystectomy (LC) has been associated with anncreased incidence of bile duct injury (BDI). There is aeneral perception that this incidence has become more than

wice that observed during the open cholecystectomy (OC)

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764 The American Journal of Surgery, Vol 195, No 6, June 2008

ra, and the currently estimated rate of BDI is .5%.1–8 Theres much debate regarding the appropriate choice of treat-ent both when BDI is recognized intraoperatively or at a

ater date. If BDI is recognized during cholecystectomy, andhe surgeon lacks experience in biliary repair, he or shehould call in a more expert surgeon for assistance 9 or drainhe surgical site and then transfer the patient to a center thatares routinely for patients with BDI. However, this rarelyappens: many unsuccessful attempts at repair are carriedut by the primary surgeon, which may complicate thenjury and aggravate the patient’s condition.1,10–13 Indeed,hese patients are often referred to a tertiary care center 1 to

weeks after the lesion has occurred, with various combi-ations of biliary fistula, biliary peritonitis, jaundice, andepsis.14

The best management of these patients may require aultidisciplinary team, including surgeons, endoscopists,

nd radiologists, to allow the most efficient diagnosticorkup and treatment. In particular, the management of

omplex proximal injuries (Bismuth types III and IV) re-uires a joint approach. This study was performed to high-ight the efficiency of BDI treatment and repair made pos-ible by a multidisciplinary approach coordinated in aertiary care surgical unit.

aterials and Methods

Between January 1994 and December 2005, 77 con-ecutive patients with BDI occurring during cholecystec-omy were treated in our tertiary care center. There were8 women and 29 men 53.4 � 14.1 years of age (mean �D). Sixty-six patients (85.7%) had major BDIs, ie, in-

uries involving the common bile duct (CBD), the biliaryonfluence, or the main bile ducts (all but 1 of theseatients were referred from other hospitals), and 1114.3%) had minor BDIs.

The prospective database used for all patients includedhe nature of the BDI (transection, partial lacerations andtrictures of the CBD, major ducts at the biliary conflu-nce, minor lesions), surgical findings at cholecystec-omy, time of injury diagnosis, initial management, re-ults of diagnostic and therapeutic procedures performedefore referral, laboratory results, imaging studies, timef referral, subsequent management, complications, andther necessary details. Follow-up consisted of periodicvaluation on an out-patient basis or by telephone inter-iew, together with laboratory tests, liver ultrasound, andagnetic resonance cholangiography (MRC) if neces-

ary. The evaluation took place every 4 months for 2ears, every 6 months for 3 years, and yearly thereafter.ean duration of follow-up after biliary repair in our unitas 48.0 � 31.7 months.Injuries were classified according to their location on the

asis of modified Bismuth classification15: type I � distance

rom biliary confluence �2 cm; type II � distance from c

onfluence �2 cm; type III � ceiling of confluence intact,ith right and left ductal systems still communicating; type

V � ceiling of confluence destroyed, with right and leftuctal systems separated; and type V � stricture of ansolated right branch associated with types I, II, or III. Ansolated injury to the right hepatic duct was classified asismuth type VI.

Events that required patient readmission and treatmentithin 30 days after discharge from our unit were consid-

red as short-term biliary complications and those occurringubsequently as long-term biliary complications. Long-termesults were classified as follows: excellent � asymptomaticatients with normal liver function tests (LFT); good �atients with normal LFT and transient symptoms orsymptomatic patients with mildly increased level of alka-ine phosphatase and gamma-glutamyl-transferase (pro-ided that the level had decreased from the preoperativeevel and that bilirubin and transaminase levels were nor-al); fair � patients with abnormal LFT with symptoms

cholangitis, pain); and poor � patients with recurrent stric-ure requiring further treatment.

esults

rimary surgery

ajor BDI. One BDI occurred in our center intraoperatively,n a patient who had already undergone surgery for liverydatidosis, during OC and was repaired immediately byoux-en-Y hepaticojejunostomy. The other BDIs occurredt other centers: 51 (51 of 65 [78.5%]) during LC and 14 (14f 65 [21.5%]) during OC. In approximately three fourths ofases, the patients had undergone surgery for acute chole-ystitis and/or the cholecystectomy was defined by the sur-eon as technically difficult.

The diagnosis of BDI was made intraoperatively in 27atients (40.9%), including the one who underwent sur-ery at our center, and the surgeon elected to proceedith immediate surgical repair in all cases. The injuryas most commonly recognized by the presence of bile in

he surgical field. Intraoperative recognition of the injuryended to occur more frequently during OC than duringC (46.7% vs 39.2%; P � not significant). The 27 im-ediate repairs were 10 Roux-en-Y hepaticojejunosto-ies (including repair of our 1 patient), 8 bile duct

econstructions over T-tube, and 9 reconstructions with-ut T-tube. In 4 of the 26 referred patients, a secondttempt at repair was performed before referral by theame surgeon who caused the BDI.

The injury was recognized postoperatively in 39 patients,nd 14 underwent subsequent surgical repair before referral:underwent Roux-en-Y hepaticojejunostomy; 5 underwent

ile duct reconstruction over T-tube; and 2 underwent re-

onstruction without T-tube.

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Overall, 40 of the 65 referred patients (61.5%) had un-ergone at least 1 attempt at surgical repair before referral:6 patients underwent Roux-en-Y hepaticojejunostomy; 13atients underwent bile duct reconstruction over T-tube; and1 patients underwent reconstruction without T-tube. Fouratients had undergone �1 attempt at repair (Table 1). Withegard to the type of injuries, these could be classified asismuth type I in 4 patients (6.1%), Bismuth type II in 15atients (22.7%), Bismuth type III in 36 patients (54.6%),ismuth type IV in 9 patients (13.6%), and Bismuth type VI

n 2 patients (3.0%) (all corresponding to Strasberg type Enjuries16) (Table 2). Five patients had concomitant vascularnjuries.

In referred patients, the time interval from cholecystec-omy to referral ranged between 1 day and 38 years (median5 days) and was �1 month in 23 patients (23 of 6535.4%]) and �12 months in 19 patients (19 of 65 [29.2%]).t the time of referral, 30 patients (30 of 65 [46.1%]) hadngoing biliary leaks, resulting in biliary ascites, biliaryeritonitis, biloma, abscess, or external biliary fistula. An-ther 15 patients (15 of 65 [23.1%]) had obstructive jaun-ice, and 20 patients (20 of 65 [30.8%]) had recurrentholangitis. The presence of biliary leak tended to be moreommon after LC (26 of 51 [51.0%]) than OC (4 of 1428.6%]) (P � NS), whereas this trend was not observed forbstructive jaundice.

Fourteen patients (14 of 65 [21.5%]) had severe sepsis oneferral and required intensive care management; 4 under-ent surgical drainage of choleperitoneum, and 10 hadultiple percutaneous drainages. Two of these patients

ied. A 66-year-old woman (Bismuth type III) was referredith choleperitoneum 3 months after open cholecystectomy

nd subsequent hepaticojejunostomy, and she died fromeptic shock shortly after referral despite surgical drainagef the abdomen. An 84-year-old woman (Bismuth type IV)as referred 40 days after open cholecystectomy with per-

utaneous biliary drainages and choleperitoneum; she hadandida albicans septicemia and developed irreversibleultiple organ failure despite drainage of the choleperito-

eum. In the other 12 patients with sepsis, definitive surgi-al BDI repair was performed after a mean of 64 days fromeferral after resolution of sepsis and recovery of a goodlinical condition.

Table 1 Attempted repairs before referral in 40 patientswith major BDIs*

Type of repair No. of patients %

Hepaticojejunostomy 16 40.0Reconstruction with T-tube 13† 32.5Reconstruction without T-tube 11 27.5Total 40 100.0

*The 1 patient with BDI that occurred in our unit was excluded.†Four patients underwent a second repair (3 for reconstruction over

T-tube and 1 for hepaticojejunostomy).

t

inor BDI. Of the 11 patients with minor BDIs, 4 casesccurred in our center, and 7 cases were referred from otherospitals. Ten lesions occurred during LC and were relatedn 4 cases to acute cholecystitis or technically difficultholecystectomy. The only BDI occurring during OC did son our center in a cirrhotic patient with portal hypertensionnd gangrenous cholecystitis (bile leak from the cystictump related to the presence of CBD stones). All BDIsonsisted of a postoperatively recognized bile leak with orithout choleperitoneum: from the cystic stump in 5 pa-

ients (in 3 cases associated with asymptomatic CBDtones), from a Lushka duct in 4 patients, and from anberrant duct for segment VI in 2 patients. Two referredatients underwent surgical drainage of the choleperito-eum before referral. Of the 11 patients with BDI, 9 hadtrasberg type A and 2 had Strasberg type C lesions.16

DI repair in our institution

ajor BDI. A total of 41 patients (41 of 64, 64.1%) under-ent surgical repair. Thirty-five of them (35 of 41 [85.4%])resented with a high BDI; 27 were classified as Bismuthevel III, 6 as Bismuth level IV, and 2 as Bismuth level VI.f the other 6 patients, 5 were Bismuth level II, and 1 wasismuth level I. The most frequently performed procedure

or repair was hepaticojejunostomy (36 of 41 [87.8%]) ac-ording to the Hepp-Couinaud technique. Of these patients,underwent multiple anastomoses performed on secondary

ile ducts. It has been our policy to place percutaneousranshepatic stents immediately before surgery in patientsith high-level injuries (Bismuth levels III to IV). In these

ases, the median duration of stenting was 4.5 months.etails of surgical procedures are shown in Table 3.Definitive treatment with biliary stenting alone was per-

ormed in 23 patients (23 of 64 [35.9%]), by endoscopicccess in 17 patients, by percutaneous access in 4, and byombined endoscopic and percutaneous access in 2. Twentyatients had stricture after surgical repair, and 3 had recentntreated injuries (1 had complete CBD transection). In 13atients (13 of 23 [56.5%]), BDI was classified as Bismuthevels I and II and in 10 patients (10 of 23 [43.5%]) asismuth levels III and IV.

Extremely relevant in the treatment of these patients was

Table 2 Level of injury in patients with major BDIsaccording to modified Bismuth classification

Bismuth classification No. of patients %

Type I 4 6.1Type II 15 22.7Type III 36 54.6Type IV 9 13.6Type V 0 0.0Type VI 2 3.0

he involvement of multidisciplinary resources with the use of

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766 The American Journal of Surgery, Vol 195, No 6, June 2008

ndoscopic retrograde cholangiopancreatography (ERCP),ercutaneous transhepatic cholangiography (PTC), andther percutaneous drainage or imaging procedures in ad-ition to the obvious need for abdominal ultrasound, com-uted axial tomography (CAT) scan, and MRC. A total of4 ERCPs were performed in 27 patients after referral: 9atients underwent 1 ERCP each, only for diagnostic pur-oses, whereas 18 patients underwent �1 ERCP each (for aotal of 55 ERCPs) for treatment or for completing otherreatments. Regarding PTC, a total of 59 examinations wereerformed in 32 patients after referral, before surgical re-air, or nonrepair: 25 patients underwent 1 PTC each (in-luding the preoperative positioning of a percutaneous bil-ary drainage before surgical repair), whereas 7 patientsnderwent �1 PTC each (with just a few simple cholan-iographic controls), yielding a total of 34 examinations forreatment or for completing other treatments.

In addition, 82 procedures were performed after sur-ery, only for assessment of the anastomoses beforeemoval of the drainage or to complete treatment. Oneatient with a Bismuth level IV lesion, after surgicalepair by small-duct anastomoses at the hilar plate, un-erwent 15 PTC with stenting to achieve successful treat-ent of segmental duct stenoses that was causing recur-

ent cholangitis.Other percutaneous procedures were of paramount im-

ortance for the treatment of sepsis from intraperitoneal oriver abscesses or other life-threatening complications ofDI. These included 3 emergency arteriographies with em-olization in 2 patients with massive hemobilia from bleed-ng pseudoaneurysms of the right hepatic artery.

inor BDI. Five patients underwent surgical drainage ofhe choleperitoneum (laparotomic in 3 patients and lapa-oscopic in 2 patients) associated with other treatmentscholedocholithotomy, positioning of T-tube or transcys-ic biliary drainage, ERCP with positioning of nasobiliaryrainage). Two patients underwent ERCP with nasobili-ry drainage (1 of them after laparotomy performed else-here); 1 patient underwent percutaneous drainage of

ocalized choleperitoneum; and 3 patients underwent pro-ressive withdrawal of abdominal drainage with sponta-eous closure of bile leaks (1 of them after laparotomy

Table 3 Type of surgical repair in 41 patients with majorBDIs

Type of repair No. of patients %

Hepaticojejunostomy at the hilar plate 36 87.8Hepaticojejunostomy 1 2.4Right hepatic duct-jejunostomy 1 2.4Right hepatectomy 2† 4.9Repair with T-tube 1 2.4

†With left hepatic duct-jejunostomy in 1 patient.

erformed elsewhere). a

esults of Repair

ajor BDI

There were no postsurgical deaths among the 41 surgi-ally repaired patients. Short-term complications occurredn 6 patients (6 of 41 [14.6%]). These included cholangitisn 2, Candida septicemia in 1, biliary fistula with intra-bdominal abscess in 1, and moderate liver insufficiency inpatients (1 case was related to right hepatectomy associ-

ted with biliary reconstruction).The outcome was excellent or good in 32, fair in 3, and

oor in 6 patients. Therefore, the rate of excellent or goodesults after surgical repair was 78.0% (32 of 41 patients).ix patients had evidence of postsurgical biliary strictureith recurrent cholangitis: 4 of them (all with initial Bis-uth levels III and IV injuries) underwent percutaneous

iliary dilatation with insertion of stents progressively in-reasing in size (up to 14F or 16F). This treatment lasted2 � 12 months (range 7 to 38), and the final result waslassified as good in all patients. The other 2 patients aretill being treated with stenting. The total percentage ofatients with excellent or good results after surgical repairlone, or after surgical repair and percutaneous stenting,as thus 87.8% (36 of 41 patients). No further surgical

epair was performed.Out of the 23 patients treated by endoscopic or percuta-

eous stenting, 17 (73.9%) had an excellent or good out-ome; in these patients the mean duration of stenting was0.7 months (range 3 to 32). Six patients are still beingreated (4 endoscopically and 2 percutaneously) after aean duration of stenting of 7.4 months (range 4 to 12).

inor BDI

In all patients, treatment allowed complete resolution ofnjury.

omments

BDI remains the most important complication of chole-ystectomy, and in past decades it has been recognized as aajor clinical challenge. Indeed, since the introduction andidespread diffusion of LC, the incidence of BDI has at

east doubled: the incidence during OC has been reported toe between 0.07% and 0.9%,17 whereas during LC it haseen reported to be between 0.16% and 2.35%.16 Thisoes not seem simply related to the “learning curve” ofC because recent studies still report a rate of BDI of.5%.18,19

Prevention of BDI is the first obvious goal. Patientshould be carefully evaluated for the presence of risk factorsefore cholecystectomy, and appropriate surgical techniquehould be employed during the surgery. Careful dissection

nd recognition of all biliary and vascular structures, before

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767G. Nuzzo et al. Multidisciplinary management of bile duct injuries

ectioning them, is of the utmost importance to preventDI. If the recognition of structures is unclear, the surgeon

hould not hesitate to convert to open technique. The role ofntraoperative cholangiography is still being debated as itas in the prelaparoscopic era.When BDI occurs, it is important to recognize the lesion

ntraoperatively. In our series, this happened in 40.9% ofatients with major BDIs (27 of 66). Indeed, this is consid-red the best time to perform repair, although several studiesave shown that a major component of success is the avail-bility of a surgeon with experience in biliary repair. Stew-rt and Way9 reported that only 17% of immediate repairs,erformed by the same surgeon who did the cholecystec-omy and who recognized the injury, were successful. In oureries, 27 patients with major BDI underwent immediateepair, and 26 of them (96.3%) had failure of the repair withubsequent referral. The selection bias in our data (figuresn successful repairs performed in primary care centersre not available) does not invalidate the concept thathances of success are increased by the availability of aurgeon who is an expert in biliary reconstruction.9,18

he success of initial repair is important because re-eated attempts at repair are significant predictors of poorutcome.13

An important component is also the availability of mul-idisciplinary facilities and expertise, which may allow ex-ct diagnosis of the lesion and contribute to treatment byonsurgical means. For these reasons, if the intraoperativelyecognized BDI occurs in a primary care center, where aurgeon trained in biliary repair and skilled interventionaladiologists and endoscopists are not available for multidis-iplinary treatment, it is preferable to simply drain thebdomen and refer the patient to a tertiary care center whereDIs are cared for routinely. In these cases, no attempt at

epair should be made because this may worsen thenjury.9,14,20,21

Also, early recognition of BDI during the postsurgicalourse is of the utmost importance. This may be relativelyasy in patients with jaundice, but it can be difficult inatients with ongoing bile leak, which was the clinicalresentation in �50% of BDI patients in the laparoscopicra.20,21 Initial symptoms may be light and nonspecific;owever, if the injury is not correctly diagnosed and treated,evere sepsis can suddenly develop. A delayed referral cane the cause of life-threatening complications as reported byameron et al14 who showed a mortality rate of 1.5% in theostinjury period caused by uncontrolled sepsis. Indeed,verwhelming sepsis was the cause of death after a complexlinical course and delayed referral in 2 of our patientsefore attempts at repair could be made. Control of sepsis ishe primary goal and should precede biliary reconstructionecause reconstruction performed during severe sepsis oreritonitis is associated with worse outcomes.14,22,23 Ag-ressive treatment of sepsis and delayed surgical repair afterecovery of good clinical condition are major components in

he control of mortality. Indeed, although we had no post- c

urgical deaths, mortality related or unrelated to sepsis is aelevant problem after surgical repair.14,18,24 We considerhe biliary repair an elective procedure to be performedeveral weeks after the resolution of sepsis, when the patientn is good general condition (Fig. 1). In our series, achieve-ent of this goal has been allowed by a multidisciplinary-anagement approach, including interventional radiolo-

ists and endoscopists, who have drained intrahepaticile ducts and intra-abdominal collections, thus helpingn the control of sepsis without early reoperation.

The surgical procedure we prefer for late repair is he-aticojejunostomy at the hilar plate. Just before surgery, welace �1 percutaneous biliary stents to obtain complete andrecise cholangiographic mapping of the lesion, to facilitatentraoperative access to the hilar structures, and–in the casef patients with complex injuries–to avoid postoperativeension on the anastomoses, and to reduce the risk of post-urgical stricture. The stent is also useful for cholangio-raphic assessment of the anastomoses. Therefore, in ourractice, preoperative placement of percutaneous stents isonsidered part of the procedure.

The availability of experienced endoscopists and radiol-gists is of paramount importance not only in the acuteanagement of septic patients but also for the definitive

reatment of those injuries that can be successfully repairedithout surgery. In our series, this occurred in 23 patientsith major BDIs (23 of 64 [35.9%]), 6 of whom are still

ontinuing treatment. Importantly, given the availability ofultidisciplinary facilities, we also avoided surgery in 3

atients with minor BDIs.The rate of excellent to good long-term results in surgi-

ally repaired patients with major BDIs was 78.0% (32 of1), and this increased to 87.8% (36 of 41) by continuingreatment with stenting in postsurgical strictures.

These data highlight the importance of a multidisci-linary approach not only to decide the best treatment forach patient but also to combine different types of treat-ent. The significance of this concept has already beenentioned in describing other phases of treatment, includ-

ng the initial assessment of BDIs and the management ofomplications, and can be applied to follow-up as well.ong-term follow-up is obviously fundamental. Indeed, annsuccessful repair with a postsurgical stricture can remainelatively asymptomatic for several years and thenresent with severe complications, such as secondaryiliary cirrhosis.

In conclusion, BDIs are serious and potentially life-hreatening complications with significant perioperativeortality. Multidisciplinary management in a tertiary care

enter with experienced hepatobiliary surgeons and avail-bility of skilled interventional radiologists and endosco-ists may offer the best options to optimize treatment. Al-hough analysis is beyond the scope of this study, theelevance of optimal management may be extended also toedicolegal and to cost-containment issues for the health

are system.

FoiPsbh

igure 1 Female patient, 34 years old, after LC converted to laparotomy because there was bile in the surgical field. She was referredn postsurgical day 13 with obstructive jaundice, acute abdomen, external biliary fistula, and systemic sepsis after ERCP with diagnosis ofnterruption of the CBD. (A) CAT scan showing choleperitoneum. (B) CAT scan–guided percutaneous drainage of choleperitoneum. (C)TC with biliary drainage (purulent cholangitis, Bismuth level III stenosis). (D) After transient recovery, recurrence of sepsis, and CATcan–guided drainage of residual biloma. The patient had a full recovery from sepsis and was discharged 36 days after referral with theiliary drainage in place. One month later, she was readmitted in good condition for elective biliary reconstruction by Hepp-Couinaud

epaticojejunostomy. (E and F) Cholangiography 45 days after reconstruction and MRC after 3 years.

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769G. Nuzzo et al. Multidisciplinary management of bile duct injuries

cknowledgments

Supported by a contribution from the Catholic Universitynd the Italian Ministry for University and Scientific Re-earch (D.1 Funds).

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