Hepatic Resection for Post-Cholecystectomy Bile Duct Injuries: a Literature Review

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provided by Elsevier - Publisher Connector DOI:10.1111/j.1477-2574.2010.00172.x HPB

REVIEW ARTICLE Hepatic resection for post-cholecystectomy bile duct injuries: a literature review

Stéphanie Truant1, Emmanuel Boleslawski1, Gilles Lebuffe2, Géraldine Sergent3 & François-René Pruvot1

1Department of Digestive Surgery and Transplantation, 2Department of Anaesthesiology and Intensive Care Medicine, 3Department of Radiology, University Hospitals, Lille, France

Abstracthpb_172 334..341 Objectives: This study seeks to identify factors for hepatectomy in the management of post- cholecystectomy bile duct injury (BDI) and outcome via a systematic review of the literature. Methods: Relevant literature was found by searching the PubMed database and the bibliographies of extracted articles. To avoid bias selection, factors for hepatectomy were analysed in series reporting both patients undergoing hepatectomy and patients undergoing biliary repair without hepatectomy (bimodal treatment). Relevant variables were the presence or absence of additional hepatic artery and/or portal vein injury, the level of BDI, and a previous biliary repair. Results: Among 460 potentially relevant publications, only 31 met the eligibility criteria. A total of 99 hepatectomies were reported among 1756 (5.6%) patients referred for post-cholecystectomy BDI. In eight series reporting bimodal treatment, including 232 patients, logistic regression multivariate analysis showed that hepatic arterial and Strasberg E4 and E5 injuries were independent factors associated with hepatectomy. Patients with combined arterial and Strasberg E4 or E5 injury were 43.3 times more likely to undergo hepatectomy (95% confidence interval 8.0–234.2) than patients without complex injury. Despite high postoperative morbidity, mortality rates were comparable with those of hepaticojejunostomy, except in urgent hepatectomies (within 2 weeks; four of nine patients died). Longterm outcome was satisfactory in 12 of 18 patients in the largest series. Conclusions: Hepatectomies were performed mainly in patients showing complex concurrent Strasberg E4 or E5 and hepatic arterial injury and provided satisfactory longterm outcomes despite high postoperative morbidity.

Keywords hepatectomy, bile duct injury, laparoscopic cholecystectomy

Received 17 November 2009; accepted 10 March 2010

Correspondence Stéphanie Truant, Service de Chirurgie Digestive et Transplantation, Hôpital Huriez, Rue M. Polonovski, CHRU Lille, 59037 Lille Cedex, France. Tel: + 33 3 20 44 42 60. Fax: + 33 3 20 44 63 64. E-mail: [email protected]

Introduction of the more proximal location of injury in the biliary tree and its frequent association with vascular injury.3 Although minor BDI, Post-cholecystectomy bile duct injury (BDI) remains a major such as leakage from the cystic duct or common bile duct, can health concern as its incidence has increased two-fold since the often be managed endoscopically, surgical reconstruction is advent of laparoscopic cholecystectomy compared with that in needed for major BDI.4,5 In most patients, repair of BDI consists of open procedures.1,2 Despite the evident learning curve, injuries immediate or delayed Roux-en-Y hepaticojejunostomy.6 In rare that occurred in laparoscopic surgery were shown to be more situations, management of these post-cholecystectomy BDIs complex than those occurring during the open procedure because requires hepatectomy.7 The aim of the present study was to Presented at the French Surgical Association Congress, 3–5 October 2007, speciﬁcally analyse, via a literature review, the factors and cir- Paris. cumstances that led to the decision for hepatectomy in the

management of post-cholecystectomy BDI. The results of such biliary reconstruction, were collected. Hepatectomies were hepatectomies were further analysed in terms of postoperative regarded as urgent when performed within the first 2 weeks. morbidity and mortality and longterm outcome. Patients who underwent liver transplantation for post- cholecystectomy BDI or hepatectomy for BDI that was not related Materials and methods to cholecystectomy were excluded from this study. Likewise, partial resection of segments IV and V to allow adequate exposure A literature search was conducted for the period 1990 to July 2008 of the bile duct9 was not considered as hepatectomy in this study. using the PubMed database, employing the search terms ‘biliary leakage and hepatectomy’, ‘bile duct injury and hepatectomy’, Statistical analysis ‘biliary stenosis and hepatectomy’ and ‘cholecystectomy and hepa- Continuous variables were expressed as means (or medians when tectomy’. The bibliographies of extracted articles were further indicated) and compared using the Mann–Whitney test. Categori- cross-referenced. Both analyses by studies and by patients were cal variables, expressed as frequencies and percentages, were com- performed to identify factors for hepatectomy. The aim of the pared using chi-squared tests or Fisher exact tests, as appropriate. analysis per study was to compare the study populations in their To identify independent factors of hepatectomy, variables identi- entirety and to search for differences in BDI features that might fied as significant in univariate analysis were subsequently explain the differences between teams in the management of these included in stepwise logistic regression analysis. The variables of BDIs. By contrast, in order to avoid selection bias, the analysis per interest were then compared among four groups of patients with: patient focused on studies that reported on same-team treatment combined arterial and Strasberg E4 or E5 injuries; isolated hepatic outcomes for patients who underwent biliary reconstruction arterial injury; isolated Strasberg E4 or E5 injury, or none of these without hepatic resection as well as patients in whom hepatic injuries. For logistic regression models, odds ratios and 95% con- resection was required with the biliary reconstruction (bimodal fidence intervals (CIs) were reported relative to a chosen reference treatment). Only studies providing information on the factors of group. Statistical significance was considered for P < 0.05. All interest, namely, the presence or absence of additional hepatic analyses were performed using spss Version 13.0 (SPSS, Inc., 8 artery injury, portal vein injury and the level of BDI (Bismuth Chicago, IL, USA). and/or Strasberg2 classification), were included. Complex BDIs were defined as proximal BDIs with disruption of the hepatic Results ductal confluence (Bismuth level 4 or 5; Strasberg type E4 or E5) or any BDI level with concurrent arterial injuries. When available, The search strategy identified 460 publications reporting various other data, such as the period of inclusion of patients or previous studies of which 31 met the inclusion criteria (Fig. 1). Of these 31

460 items Excluded Other complications post- cholecystectomy n = 52 BDI from other causes n = 30 Post-cholecystectomy BDI n = 378 Prevalence of BDI n = 81 Risk factors and prevention of BDI n = 130 Management of post- cholecystectomy BDI n = 167

Imaging of BDI n = 30

Treatment of post- n cholecystectomy BDI = 137 Biliary repair for BDI (surgical and/or endoscopic and/or radiological) n = 113

Hepatectomy for post- Liver transplantation for BDI n = 3 cholecystectomy BDI n = 21

Cross-referenced Hepatectomy for bibliographies of post-cholecystectomy BDI n = 31 extracted articles

Figure 1 Flow chart showing details of articles selected from the PubMed database, subsequent exclusions and cross-referenced bibliographies of extracted articles. BDI, bile duct injury

studies, 10 were case reports and 21 were retrospective series. For pared with urgent (within 2 weeks) hepatectomy (2/53 vs. 4/9 three teams, patient(s) undergoing hepatectomy were reported on patients; P = 0.003). With regard to longterm outcome, the largest twice;9–14 those patients were pooled and considered as one study series14 reported that 13 of 18 patients who underwent hepatec- for each team. Among other extracted articles that reported on tomy for complex BDI had no symptoms after a median follow-up only biliary repair with no hepatectomy, 31 studies that provided of 8 years (range 3–12 years) (Table 2). enough information on the factors of interest described above were used as a control group in the analysis per study. Comparison of patient features between series reporting bimodal treatment and control studies Analysis per study When the study populations were considered in their entirety, the Study population 21 series reporting bimodal treatment were found to be compa- Altogether, 99 patients who underwent hepatectomy for post- rable with the 31 control studies in terms of laparoscopic cholecystectomy BDI (12 in case reports, 87 in the series reporting approach (75.4% [range 23–100%] vs. 76.3% [range 0–100%], bimodal treatment) were identified in a total of 1756 patients respectively; P = 0.60) and periods of inclusion (median time of (5.6%) and are summarized in Table 1. Overall, 91.5% (65/71 inclusion before the year 2000 in 90.5% vs. 90.6%; P = 1.00). By patients in 22 studies) of hepatectomies were performed after contrast, when the 21 series reporting bimodal treatment were laparoscopic cholecystectomy. For anatomical reasons, right compared with the 31 control studies, the incidences of hepatic lobectomy was the most frequently performed hepatectomy arterial injury (22.3% [range 0–100%] vs. 13.0% [range (n = 79/99, 79.8%) (Table 1). In the 21 series reporting bimodal 0–61.1%], respectively; P < 0.001], portal vein injury (1.0% treatment, the median (range) incidence of hepatectomy was [range 0–6.7%] vs. 0.1% [range 0–3.4%], respectively; P = 0.047), 6.1% (1–20%) of all patients referred for BDI, with a median complex BDI (26.5% [range 17.8–100%] vs. 21.7% [range number of three (one to 18) hepatectomies per series (Table 1). 0–100%], respectively; P = 0.01) and previous biliary reconstruc- Previous biliary reconstruction had been performed in 71.2% tion (46.0% [range 0–100%] vs. 41.4% [range 0–100%], respec- (47/66) of patients. tively; P = 0.042) were significantly higher. The frequency of vascular injury, severity of biliary injury and timing of hepatectomy are shown in Table 1. In nine patients, urgent hepatectomy (within 2 weeks) was needed in cases of Analysis per patient parenchymal necrosis caused by combined biliary and vascular Among the 21 studies reporting bimodal treatment, eight19,28,30–35 injury following laparoscopic cholecystectomy (Table 1). Substan- provided enough detail per patient on the variable of interest, tial variations existed in the indications mentioned for postponed which included: injury of the hepatic artery and/or portal vein; hepatectomy, as follows: recurrent biliary sepsis;12,15 biliary stric- proximal pattern of BDI (Strasberg E4 or E5 injury), and, to a tures caused by continuous cholangitis;12,16,17 development of lesser extent, previous biliary reconstruction. Other potential intrahepatic abscesses;18,19 non-visualization and/or unsuitability factors, such as referral pattern, and presence or absence of sepsis of the proximal stump of the injured bile duct(s) for anastomo- or lobar atrophy, could not be assessed, as insufficient data were sis;9,20,21 intrahepatic injuries of an aberrant right hepatic duct;20 provided. Data were collected from these eight studies for a total anastomotic strictures and intrahepatic lithiasis;21,22 right hepatic of 233 patients and results are shown in Table 3. One patient was lobe atrophy with23,24 or without10,21 recurrent cholangitis; second- excluded from analysis as he underwent liver transplantation. ary biliary cirrhosis;11,12 hepatic confluence stented with metallic Logistic regression models were performed for 182 patients for stents,14,25 or primary non-diagnosed Klatskin tumour.26 Such whom data on all the variables of interest were available; results indications were related to symptoms in all patients. are shown in Table 4.

Postoperative morbidity, mortality and Discussion outcome of hepatectomies Rates of postoperative morbidity were high, mainly secondary to Overall, 99 hepatectomies have been reported thus far in the man- infectious complications14,21,27 (Table 2). In one series of 18 agement of post-cholecystectomy BDI. This review is the first to patients, despite the use of intermittent portal trial clamping in 14 show that proximal biliary injuries with disruption of hepatic patients (78%), 12 patients required a blood transfusion for a ductal confluence (Strasberg types E4 or E5) and/or concurrent mean of 6 Ϯ 3.6 units (range 2–12 units).14 Biliary fistula occurred arterial injuries are independent factors for hepatectomy in the in 25% (3/12)28 to 39% (7/18)14 of patients. One study also management of post-cholecystectomy BDI. Among 31 studies, reported a longer hospital stay than that found among patients 92.6% of 99 patients undergoing hepatectomy had an underlying who underwent hepatectomy for other reasons.29 Postoperative complex BDI. Patients with combined arterial and Strasberg death following hepatectomy occurred in 11.1% (9/81) of patients E4 or E5 injuries were at particular risk of hepatectomy, with an for whom data were available. Nevertheless, mortality was signifi- odds ratio of 43.3 (95% CI 8.0–234.2) (Table 4), compared with cantly lower in those undergoing non-urgent hepatectomy com- patients with none of these complex injuries.

Author Year Patients, Vascular injury Complex Time of Definitive treatment n/totala b (%) RHAI PVI injuries , n hepatectomy Branum et al.16 1993 2/50 (4) NS NS 2 NS Right lobectomy Madariaga et al.34c 1994 2/15 2 1 2 5/21 days Right lobectomy Ohtsuka et al.20 1999 10 0 0 1 4 months Right lobectomy Nishio et al.15 1999 10 1 1 1 135 days Right lobectomy Topal et al.24 1999 1/16 0 0 1 NS Left lateral sectionectomy Uenishi et al.23 1999 10 1 0 1 13 months Right lobectomy Lichtenstein et al.33c 2000 2/16 0 0 2 4/28 days Segment V–VI resection Nishiguchi et al.51 2000 10 0 0 1 13 months Right lobectomy Gazzaniga et al.22 2001 1/60 (1.7) NS NS NS NS Left lateral sectionectomy Kayaalp et al.48c 2001 20 2 0 2 4–15 days Right lobectomy Wong et al.52 2001 1 1 1 1 5 weeks Right lobectomy Buell et al.32 2002 3/49 3 0 3 NS Right lobectomy Heinrich et al.53c 2003 10 0 1 1 2 weeks Right lobectomy Schmidt et al.11,12 2002–2004 3/54 (5.5) 3 0 3 NS, 4, 8 months Right lobectomy Frilling et al.26 2004 5/40 4 0 4 NS Right lobectomy Ota et al.17 2004 10 0 0 1 144 days Right lobectomy Sekido et al.19 2004 2/10 2 0 2 2.5/5 months Right lobectomy Stewart et al.43 2004 4/261 (1.5) 4 0 4 NS Partial lobectomy (3), right lobectomy (1) Mercado et al.9 2006 3/285 (1.1) NS NS 3 NS Right lobectomy De Santibanes et al.27 2006 9/169 (5.3) NS NS 9 NS Right lobectomy (7) or left hepatectomy (2) Felekouras et al.54c 2007 10 1 1 1 1 day Right lobectomy Yan et al.35 2007 1/8 1 0 1 NS Right lobectomy 00ItrainlHpt-acet-iir Association Hepato-Pancreato-Biliary International 2010 © Wu et al.55 2007 2/210 (1) NS NS NS NS Right lobectomy Li et al.56 2007 3/60 (5) 3 0 3 NS Right lobectomy Ragozzino et al.57c 2007 20 2 2 2 2–3 days Right lobectomy Ortega-Deballon et al.31c 2007 1/18 1 0 1 NS Right lobectomy Bektas et al.28 2007 12/74 (16.2) 6 3 7 NS Right lobectomy (10), segmentectomy (2) Thomson et al.21 2007 8/119 (6.7) 4 1 7 6–95 months Right lobectomy (6), left lateral sectionectomy (2) Alves et al.10 2003–2008 18/120 (15) 11 4 18 7 days to 21 years Right (14) or left (3) lobectomy or left trisectionectomy (1) Laurent et al.14 Nuzzo et al.58 2008 2/77 (2.6) NS NS NS NS Right hepatectomy Truant et al.30 2009 3/45 1 0 3 8, 18, 30 years Right lobectomy (2) or left hepatectomy (1) Total 99/1756 (5.6) 53/80d (66.3%) 15/80d (18.8%) 87/94d (92.6%) Right lobectomy

aTotal number of patients referred for bile duct injury bComplex injuries were defined as proximal biliary injuries with disruption of the hepatic ductal confluence (Bismuth level 4 or 5; Strasberg type E4 or E5) or any biliary level injury with concurrent arterial injuries cUrgent hepatectomy dTotal including only patients for whom information was specified 337 RHAI, right hepatic artery injury; PVI, portal vein injury; NS, not specified 338 HPB

Table 2 Postoperative morbidity, mortality and outcome of hepatectomy in the management of post-cholecystectomy bile duct injury Author Year Patients, n Complex Morbidityb, Mortalityb, Longterm outcome injuriesa, n n n Madariaga et al.34c 1994 2 (1c) 2 – 0 Good at 14–16 months Uenishi et al.23 1999 1 1 – 0 Good at 22 months Lichtenstein et al.33c 2000 2 (1c) 2 – 0 Good at 12–13 months Kayaalp et al.48c 2001 2 (2c) 2 – 1 Good at 3 years (one postoperative death) Buell et al.32 2002 3 3 NS 2 NS Schmidt et al.11,12 2002–2004 3 3 NS 1 Good at 39 months/SBC at 83 months (one postoperative death) Heinrich et al.53c 2003 1 1 – 0 – Ota et al.17 2004 1 1 – 0 Good at 5 years Sekido et al.19 2004 2 2 – 0 No symptoms at 16–36 months Frilling et al.26 2004 5 4 NS 1 NS De Santibanes et al.27 2006 9 9 3 0 NS Yan et al.35 2007 1 1 – 0 Normal postoperative liver function Li et al.56 2007 3 3 NS 1 No symptoms at >12 months (one postoperative death) Felekouras et al.54c 2007 1 1 – 1 – Ragozzino et al.57c 2007 2 (2c)2 – 1 – Thomson et al.21 2007 8 7 5 0 Good in 8/8 (time of follow-up not specified) Ortega-Deballon et al.31c 2007 1 1 – 1 – Alves et al.10 2008 18 18 11 0 No symptoms in 13/18 patients; median (range) Laurent et al.14 follow-up: 8 (3–12) years Truant et al.30 2009 3 3 2 0 Good at 13, 17, 63 months aComplex injuries were defined as proximal biliary injuries with disruption of the hepatic ductal confluence (Bismuth level 4 or 5; Strasberg type E4 or E5) or any biliary level injury with concurrent arterial injuries bNumber of complication(s) and death(s) are given for studies reporting at least three cases of hepatectomy cUrgent hepatectomy (when more than one hepatectomy were performed, the number of urgent hepatectomies is given in parentheses in the Patients, n column) NS, not specified; SBC, secondary biliary cirrhosis

Table 3 Univariate analysis: comparison of patients who underwent hepatectomy with patients who underwent biliary repair in series reporting bimodal treatment n (%) No hepatectomy (n = 206), n Hepatectomy (n = 26), nP-value Artery injury 45 (19.3) 29 16 <0.001 Portal vein injury 5 (2.1) 1 4 0.001 Strasberg E4 or E5 injury 25/182a (13.7) 15/158a 10/24a <0.001 Previous biliary reconstruction 65/158a (41.1) 56/144a 9/14a 0.06 aMissing data for remaining patients

Overall, 91% (91/99) of hepatectomies performed for the man- ficult to repair with uncertain outcome. Overall, there were sig- agement of post-cholecystectomy BDI were reported after the year nificant differences in the rates of concomitant vascular injuries 2000 – one decade after the advent of laparoscopic cholecystec- and complex injuries between teams reporting hepatectomies per- tomy – and were carried out mostly by teams specializing in formed in the management of BDI patients and those performing hepatobiliary surgery (Table 1). This strongly contrasted with biliary repair exclusively by hepaticojejunostomy. The enhanced older series reported by specialist hepatobiliary surgery teams,36 complexity of BDI has certainly impacted the decision to perform but also with recent series3,37–39 reporting no hepatectomy despite hepatectomy in this setting. concomitant vasculo-biliary injuries with or without lobar Indeed, in recent years, certain teams have deliberately chosen atrophy. This new indication for hepatectomy may reflect the to perform hepatectomy in patients with complex laparoscopic specific complexity of laparoscopic BDI, which is considered dif- BDI for reasons related to the excellent longterm outcome of

Table 4 Multivariate analysis of 182 patients (hepatectomy: n = 23; biliary repair: n = 159) for whom data on all the variables of interest (hepatic artery injury, portal vein injury and Strasberg E4 or E5 injury) were available Factors P-value Hepatectomy

OR 95% CI for OR Hepatic artery injury Yes vs. no <0.001 7.7 2.6–22.4 Portal vein injury Yes vs. no 0.1 6.9 0.6–75.7 Strasberg E4 or E5 injury Yes vs. no 0.003 5.7 1.8–17.9 Complex injury No hepatic artery, no Strasberg E4 or E5 injury 1.0 – Isolated artery injury <0.001 14.9 4.3–51.6 Isolated Strasberg E4 or E5 injury <0.001 11.8 2.9–47.2 Artery + Strasberg E4 or E5 injury <0.001 43.3 8.0–234.2

A separate logistic regression model was used to evaluate the independent effect of complex injury, (hepatic artery injury or Strasberg E4 or E5 injury, or both), in comparison with the group with neither hepatic artery nor Strasberg E4 or E5 injury OR, odds ratio; 95% CI, 95% confidence interval

hepatectomy.14 In the present review, rates of good or excellent (no requires more substantial dissection in the pedicle, with subse- symptoms) results of hepatectomy series, which ranged from 72% quent damage to the vascularization of the bile duct.36,42 Stewart (13/18) to 100% (8/8) in the two largest series,14,21 were compa- et al.43 studied the impact of injury propagation in successive rable with those obtained in most series of BDI patients treated by operations (i.e. the increase in the proximal extent of the BDI hepaticojejunostomy.3,36,40,41 By contrast, given the expected diffi- between initial injury and subsequent successful reconstruction) culties in dissection of such hepatectomies and their high mor- upon the incidence of hepatic arterial injury. For injuries located bidity rates, which are higher than those reported in the literature at or above the bifurcation of the common hepatic duct, 49% of for biliary repair, it is likely that additional factors were taken into those without injury propagation had right hepatic artery injury account in the choice of this treatment. in comparison with 71% of those with injury propagation In fact, most indications for performing hepatectomy were (P < 0.05). These authors further showed that the need for hepa- encountered in patients displaying concurrent arterial and proxi- tectomy was more common among patients with arterial injury mal injuries with disruption of the hilar confluence, with an than among those without such injury, but only in patients in odds ratio for hepatectomy of 43.3 (95% CI 8.0–234.2) whom biliary repair had been performed by a surgeon who was (Table 4), in comparison with patients with neither arterial nor inexperienced in hepatobiliary repair.43 These data underline the proximal Strasberg E4 or E5 injury. Indeed, over the longterm, importance of early referral to a tertiary centre in BDI patients, as such complex concomitant vasculo-biliary injuries were shown previously reported.44 to compromise the viability of biliary ducts and/or parenchyma By contrast, when the biliary confluence was preserved, patients of the hemi-liver because confluence disruption impaired the with and without hepatic arterial injuries had comparable long- development, within the hilar plate, of omega-shaped collateral term outcomes, provided that high-level repair using the Hepp– arterial circulation originating from the preserved branch of the Couinaud technique45 was performed to guarantee non-ischaemic hepatic artery.10 In this setting, the justification for partial hepa- bilioenteric anastomosis.10,36,38 Over one-third of patients with tectomy was based on the danger of irreversible fibrotic and injuries for which Strasberg E4 or E5 classification was the only atrophic parenchyma, with high risk for secondary complica- criterion of gravity underwent hepatectomy, which appears high tions such as persistent cholangitis as a result of vascular or despite the fact that the integrity of the hilar confluence was septic lesions. In accordance with the findings of this study, one shown to be important in predicting postoperative biliary stric- recent study of 74 BDI patients showed that the type of vascular ture.4,9,38 With respect to the Hepp–Couinaud technique, hepate- involvement and the location of the lesion, at or above the bifur- ctomy for Strasberg E4 or E5 BDIs should not be indicated in cation of the hepatic duct, had a major impact on the extent of patients without fibrosis or significant vascular compromise surgical intervention for iatrogenic BDI and especially the need except in rare cases when high-quality biliary repair is difficult or for hepatectomy.28 even impossible, such as when segmental bile ducts are either For similar reasons, the need for hepatectomy was associated, in constricted as a result of persistent cholangitis or are unsuitable the present study, with a higher rate of previous biliary recon- for anastomosis.9,17,20 As alternative approaches, side-to-side struction, with a trend towards significance when compared with hepaticojejunostomy on separated right and left ducts,46 or partial patients who had biliary repair (P = 0.06) (Table 3). Each failed resection of segments IV and V to enable adequate exposure of the repair is indeed associated with some loss of bile duct length and left and right ducts,47 have been proposed.

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