1. Treatment of failed Roux-en-Y hepaticojejunostomy after post-cholecystectomy bile ducts injuries Amine Benkabbou, MD,a Denis Castaing, MD,a,b,c Chady Salloum, MD,a Ren Adam, MD, PhD,a,c,d e Daniel Azoulay, MD, PhD,a,c and Eric Vibert, MD, PhD,a,b,c Villejuif, France Background. Roux-en-Y hepaticojejunostomy (RYHJ) is the most well-accepted treatment for most post- cholecystectomy bile duct injuries (BDI). RYHJ failure is a complex situation that requires expert planning and the possibility of using a combination of operative, radiologic, and endoscopic techniques. The aim of this study was to report our experience with a multidisciplinary approach to failed RYHJ after post-cholecystectomy BDI. Methods. Between January 1996 and March 2008, 44 consecutive patients were managed for RYHJ failure in our department. They presented with recurrent cholangitis in 40 patients (91%) and/or jaundice in 9 (20%). First-line treatment consisted of primary revisionary surgery in 26 cases (59%; repeat RYHJ in 22 and hepatectomy in 4) and a percutaneous approach in 18 cases (41%; biliary interventions in 16 and portal vein embolization in 2). Results. Postoperative mortality was nil. Postoperative morbidity was 11% after repeat RYHJ without hepatectomy, 80% (bile leaks) after hepatectomy, and 10% (mild cholangitis and hemobilia) after a percutaneous approach. Delayed revisionary surgery with the intent to wait for bile duct dilation failed in all 5 patients. With a mean follow-up of 49 ± 40 months, second- or third-line treatment was attempted in 7 patients (16%). One patient (2%) died because of suicide. Overall clinical success deﬁned by the absence of incapacitating biliary symptoms after treatment was achieved in 39 patients (89%). Conclusion. An immediate, multidisciplinary approach including repeat biliary surgery and/or a percutaneous approach in a tertiary hepatobiliary center is required to obtain good, long-term results when treating the failure of RYHJ post-cholecystectomy BDI. (Surgery 2013;153:95-102.) From the AH-HP,a H^pital Paul Brousse, Centre Hpato-Biliaire, Inserm,b Unite 785, the Universit o e e Paris-Sud,c and Inserm,d Unite 776, Villejuif, FranceROUX-EN-Y HEPATICOJEJUNOSTOMY (RYHJ) is the stan- of this complex situation requires careful and ex-dard treatment for most post cholecystectomy bile pert management and the possibility of having aduct injuries (BDI) with long-term clinical success combination of operative, radiologic, and endo-rates reaching 90%.1 Some patients who undergo scopic techniques. Few reports have speciﬁcallyRYHJ for BDI will experience incapacitating biliary analyzed the results of failed biliary repairs forsymptoms, such as jaundice or recurrent cholangi- post-cholecystectomy BDI.2-6 The aim of our studytis.2 However, in addition to anastomotic stricture, was to evaluate the short- and long-term results ofseveral other, isolated or associated pathogenic fac- a multidisciplinary approach regarding failedtors for RYHJ failure include intrahepatic calculi, RYHJ after post-cholecystectomy BDI.intrahepatic stricture, and improper technicalconstruction of the Roux-en-Y limb. Management PATIENTS AND METHODS Between January 1996 and March 2008, 44Accepted for publication June 14, 2012. consecutive patients were treated in our depart-Reprint requests: Eric Vibert, MD, PhD, 12 avenue Paul Vaillant ment (Centre Hpato-Biliaire, Paul Brousse Hos- eCouturier, 94804 Villejuif Cedex, France. E-mail: eric.vibert@ pital, Assistance Publique des Hopitaux de Paris,pbr.aphp.fr. Villejuif, France) for the failure of RYHJ per-0039-6060/$ - see front matter formed because of post-cholecystectomy BDI.Ó 2013 Mosby, Inc. All rights reserved. Our group of patients comprised 13 males (30%)http://dx.doi.org/10.1016/j.surg.2012.06.028 and 31 females (70%) with a mean (± SD) age of SURGERY 95
2. 96 Benkabbou et al Surgery January 2013Table I. Serum biochemistry ﬁndings at referral Normal range Median Min MaxPT (%) 70 94 68 100Bilirubin (mmol/L) 17 13 5 134AP (UI/L) 120 183 123 1,128GGT (UI/L) 50 210 52 2,074AST (UI/L) 35 48 15 491ALT (UI/L) 43 62 9 776Creatinine (mmol/L) 18–106 64 47 140Protein (g/L) 60–80 71 48 80Albumin (g/L) 38 41 29 50Leukocytes (N./mL) 4,800–10,800 6,150 3,240 14,800Hemoglobin (g/dL) 12–16 12.9 8 15.8Platelets (N.103/mL) 150–400 256 85 658ALT, Alanine aminotransferase; AP, alkaline phosphatase; AST, aspartate aminotransferase; GGT, gamma glutamyl transferase; PT, prothrombin time.51 ± 14 years (range, 17–78). All BDI were abnormalities were present (Table I). Leukocytosissustained during cholecystectomy performed and thrombocytopenia were present in 3 patientsfor cholecystolithiasis. The approach for the cho- (7%) and 1 patient (2%), respectively.lecystectomy was laparoscopic in 35 patients (80%) Vascular and liver parenchymal assessmentsand open in 9 patients (20%). The level of BDI was (Table II) were performed using routine abdominalassessed according to Bismuth’s classiﬁcation (7): ultrasonography and computed tomography of theType 1 in 2 patients (5%), type 2 in 18 (41%), type liver with intravenous contrast. These imaging mo-3 in 12 (27%), type 4 in 5 (11%), and type 5 in 7 dalities revealed liver atrophy in 7 patients (16%),(16%). The time elapsing between BDI and initial and evidence of injury to the main (2 patientsrepair (RYHJ) was a median of 6 days (range, 0– [4%]) or right branch (6 patients [14%]) of the he-703). The initial repair was performed very early patic artery injury in 8 patients (18%). Liver atrophy(48 hours) in 9 patients (20%), early (45 days) and vascular injury were both present in 2 patients.in 22 (50%), and delayed (45 days) in 13 (30%). Biliary assessments were performed using per-The BDI was incurred and the failed RYHJ was cutaneous cholangiography in 34 patients (77%)performed in the same hospital in 34 patients and/or magnetic resonance cholangiography in 23(72%). Before referral to our department, an (52%). These procedures revealed intrahepaticinitial revisionary operation for the failed RYHJ calculi in 18 patients (41%) and bile duct dilationwas performed in 10 patients (23%), and involved in 11 (25%). The level of obstruction was suspecteda hepaticojejunostomy repair in 3 patients, Roux- to be hilar or suprahilar in 39 patients (89%).en-Y limb repair in 2 patients, and percutaneous Treatment strategy was deﬁned at a multidisci-dilatation of a stricture in 5 patients. These 10 plinary staff meeting including surgeons, radiolo-patients were referred to our department because gists, and hepatogastroenterologists during aof persistent biliary symptoms despite this revision- case-by-case analysis in our tertiary center that offersary operation. different multidisciplinary approaches to hepato- The patients were admitted to our department biliary disorders (operative, endoscopy and inter-for recurrent cholangitis in 40 patients (91%) ventional radiology). The treatment strategyand/or jaundice in 9 (20%). Recurrent cholangitis comprised 2 types of treatments: Revisionary sur-was deﬁned as fever 388C or episodic right upper gery, including a revision of hepaticojejunostomyquadrant pain with no identiﬁable source outside and/or hepatectomy, or a percutaneous approach,the hepatobiliary system occurring a minimum of 3 including biliary maneuvers and/or portal veintimes in the preceding year. Continuous or inter- embolization. These treatments were performedmittent biliary symptoms had developed within a alone or in combination and subsequently deﬁnedmedian period 4 months (range, 0–204) since the the different lines of treatment in the same patient.pre-referral procedure. An external biliary drain Revisionary surgery was considered in patientswas present in 7 patients (16%), and no patient in good general condition without uncontrolledhad an active bile leak. biliary sepsis and was designed to perform an end- Cholestasis had been present in all patients. No to-side, wide, healthy, mucosa–mucosa hepaticoje-major coagulation and renal function junostomy without tension and with a 70-cm long
3. Surgery Benkabbou et al 97Volume 153, Number 1Table II. Radiologic ﬁndings at referral bile duct. A hepatotomy between segments 5 and 4 Findings n through of the bed of the gallbladder was used to access the secondary right biliary conﬂuence.Calculi 18 (41%) Visual magnifying aids were used routinely toBile duct dilation 18 (41%) optimize biliary dissection, the recognition of Bilateral 11 healthy mucosa, and the anastomoses. These anas- Left liver 4 Right liver 1 tomoses were performed using 5/0 or 6/0 inter- Right sector 2 rupted, nonabsorbable, monoﬁlament sutures withVascular injury 8 (18%) the knots tied on the external surface of the Right branch of hepatic artery 6 anastomosis. An ultrasonic dissector and bipolar Hepatic artery 2 coagulation forceps were used routinely during anyParenchymal liver atrophy 7 (16%) hepatectomy. Right liver 5 Percutaneous approaches. All percutaneous Left lateral lobe 1 procedures were carried out in the operating Segment 4 1 room under full aseptic conditions as applicableLevel of biliary obstruction to any operative procedure.7 The operating suite Infrahilar 5 (11%) was equipped with a Doppler Ultrasound (Aloka Hilar 25 (57%) Suprahilar 14 (32%) SSD 680, Aloka, Tokyo, Japan) and a light ampli- ﬁer (Diasonics 3800; Diasonics, Milpitas, CA). These procedures were performed under either local anesthesia, neuroleptic analgesia with pre-retrocolic Roux-en-Y limb. In patients with a lon- medication, or general anesthesia with intubationgitudinal stricture extending into the intrahepatic if the duration of the procedure was expected tobile ducts, associated with liver atrophy, a hepatec- be of a greater duration. Biliary maneuvers con-tomy was performed with or without RYHJ revi- sisted of 3 successive stages: Establishing adequatesion. A percutaneous approach was considered in transhepatic and/or transjejunal8 access to thepatients with a (1) marked worsening in their biliary tract if not present, performing the re-general condition or hepatic function, or severe quired intervention, and obtaining a contrastsepsis, all of which contraindicated an operative study to demonstrate if the procedure was success-procedure, (2) a local contraindication at the level ful. When necessary, endoscopic control of theof the bile duct owing to a cavernous transforma- procedure was ensured using a pediatric broncho-tion of a thrombosed portal vein or after numer- scope (diameter, 4 mm). Strictures were treatedous previous biliary interventions, or (3) an by balloon dilatation and calculi by extractionisolated short intra-hepatic biliary stricture.7 Portal and/or lithotripsy (Lithotron EL27, Walz Elektro-vein embolization was performed in patients with nik GMBH, Germany). Portal vein embolizationan isolated longitudinal intrahepatic biliary stric- was performed via a transhepatic approach.ture in attempt to induce parenchymal atrophy Follow-up data were obtained by means ofin the distribution of the diseased bile ducts. review of hospital and outpatient records. All Techniques of revisionary surgery. An end-to- patients were seen 1 month after hospital dis-side, wide, healthy, mucosa–mucosa hepaticojeju- charge and underwent computed tomographynostomy without tension and with a 70-cm long and a complete biochemical assessment. Thereaf-retrocolic Roux-en-Y limb was the goal in each ter, they were followed with liver ultrasonographypatient. Operative exploration consisted of 3 stages: every 4 months during the ﬁrst year and every 6Veriﬁcation of the erroneous construction of the months for 2 years, and the yearly thereafter.Roux-en-Y limb, exposure of the anastomotic area Postoperative morbidity was assessed according towith collection of a sample of bile, and assessment the Clavien-Dindo classiﬁcation.9 Clinical outcomeof biliary anatomy and/or abnormalities (calculi, was determined according to the Terblanche classi-stricture) using intraoperative cholangiography. ﬁcation10: grade I, no biliary symptoms; grade II,When feasible in patients with intra-hepatic bile transitory symptoms and no current symptoms;duct dilation, a preoperative transhepatic cholan- grade III, biliary symptoms requiring medicalgiography followed by transhepatic biliary drainage therapy; and grade IV, recurrent biliary symptomswas performed. Intraoperatively, this drainage was requiring correction or related to death. Ter-very useful in localizing the bile duct after removal blanche class IV constituted a poor result. Ter-of the RYHJ and dissecting the hilar plate to expose blanche I, II, and III constituted a clinical successthe primary biliary conﬂuence and notably the left with excellent, good, and fair results, respectively.
4. 98 Benkabbou et al Surgery January 2013RESULTS thus optimize revision. None of these patients The mean (± SD) follow-up period was 49 ± 40 developed bile duct dilation after a mean ofmonths (range, 2–153). One patient (2%) died as waiting time of 20 ± 17 months. During this period,a result of suicide 44 months after the initial 4 patients developed recurrent cholangitis. Liverhepatectomy. In 7 patients (16%), $2 treatments abscess and pylephlebitis of the right portal branchwere required, with a mean follow-up of 33 ± 36 occurred in 1 patient with a previous injury of themonths (range, 2–85). At the time of last follow- right branch of the hepatic artery.up, clinical success had been achieved in 39 Revisionary surgery without hepatectomy (n = 26 pro-patients (89%): 34 patients (77%) were asymptom- cedures in 25 patients): Revisionary surgery withoutatic (Terblanche I–II), and 5 patients (11%) had hepatectomy was performed as ﬁrst-line treatmentexperienced an improvement in their symptoms in 22 patients, as second-line treatment in 3(Terblanche III). The overall result was poor patients (after a percutaneous approach), and as(Terblanche IV) in 5 patients (11%). An overview third-line treatment in 1 patient (after revisionaryof the results is shown in Fig 1. First-line treatment surgery followed by a second-line percutaneous(Fig 2) consisted of primary revision surgery (ﬁrst- approach). Morbidity occurred after 3 of 26 pro-line revisionary surgery) in 26 patients (59%) and cedures (11%): Abdominal hematoma manageda percutaneous approach (ﬁrst-line percutaneous with transfusion in 1 patient (Clavien-Dindo II),approach) in 18 patients (41%). cholangitis managed with antibiotics in 1 (Clavien- First-line revisionary surgery (n = 26 [59%]; Dindo II), and acute pancreatitis that requiredTable III). The Roux-en-Y limb was found to be exploratory laparotomy for suspected biliary peri-short (70 cm) in 12 patients (44%) and was re- tonitis in 1 (Clavien-Dindo IIIb).modeled to a length of 70 cm. Revisionary surgery Revisionary surgery with hepatectomy (n = 5 proce-included repeat hepaticojejunostomy in 23 patients dures in 4 patients): Hepatectomy was performed(89%), which involved more than a single duct in as ﬁrst-line treatment in 4 patients and as second-13 (54%; (range, 1–5). In 3 patients (11%), revi- line treatment in one who underwent operationsionary surgery was suboptimal because an anasto- twice. Bile leaks occurred after 4 proceduresmosis of the isolated right sector duct (1 case) or (80%). Morbidity occurred as Clavien-Dindo IIsegment 4 duct (2 cases) was impossible. Drains after 3 procedures and Clavien-Dindo IIIb afterwere placed through the hepaticojejunostomy in 4 1 ﬁrst-line procedure complicated by a bilio-patients (17%). An access limb of jejunum was pleural ﬁstula managed with prolonged drainageplaced under the abdominal wall to enable subse- that progressed to a chronic external ﬁstula re-quent percutaneous access in 3 patients (13%). quiring repeat hepatectomy.Hepatectomy was performed in 4 patients (15%) in- Percutaneous approach (n = 120 procedures in 21 pa-cluding 2 right hepatectomies, 1 left hepatectomy, tients): A percutaneous approach was adopted asand 1 left lateral sectionectomy). ﬁrst-line treatment in 18 patients and as addi- First-line percutaneous approach (n = 18 [41%]; tional treatment in 3 (after initial revisionaryTable IV). Access to the biliary tract was established surgery). In 1 patient, additional treatment con-by catheterization of the jejunal limb (the ‘‘cul-de- sisted of a combination of biliary maneuvers andsac’’) in 9 patients (54%), transhepatic catheteriza- right sectoral portal vein embolization. There wastion in 4 patients (23%), or combined techniques no mortality. No morbidity was observed afterin 4 (23%). The procedures were performed un- portal vein embolization. Hemobilia that did notder biliary endoscopic control in 12 patients require a blood transfusion (Clavien-Dindo I)(27%). Balloon dilatation of a stricture, extraction and/or cholangitis managed with IV antibioticsof calculi and/or biliary cast, and lithotripsy were (Clavien-Dindo I) occurred after 10% of theperformed in 12 (70%), 8 (47%), and 4 patients biliary interventions.(23%), respectively. In 2 patients with calculi, su- Long-term results. Revisionary surgery withouttures exposed in the bile duct lumen were re- hepatectomy (n = 22 patients): Satisfactory primarymoved percutaneously under endoscopic control results were achieved in 18 patients (82%): 17via access of the jejunal limb. Transhepatic portal patients (94%) became asymptomatic (Terblanchevein embolization was performed in 2 patients I–II) and 1 patient (6%) improved, although with(right posterior sectoral portal branch and right some symptoms (Terblanche III). In 4 patientsportal branch). (9%), the symptoms did not improve (Terblanche Short-term results. In 5 patients (20%), ﬁrst-line IV). One of these patients experienced generallyrevisionary surgery was delayed at referral in at- fair results (Terblanche III) after an additionaltempt to wait for bile duct dilation to develop and percutaneous approach.
5. Surgery Benkabbou et al 99Volume 153, Number 1Fig 1. Overview of the results as a function of the Terblanche classiﬁcation of 44 patients, achieved with 1, 2 or 3 step(s).HJ, Hepaticojejunostomy; PVE, portal vein embolization; T, Terblanche classiﬁcation10; TI, no biliary symptoms; TII,transitory biliary symptoms, no current symptoms; TIII, biliary symptoms requiring medical therapy; TIV, recurrent bil-iary symptoms requiring correction or related to death. and 4 (29%) had improvement in their symptoms (Terblanche III). In 2 patients (6%), the symptoms were not primarily improved (Terblanche IV), but both became asymptomatic (Terblanche I–II) after further revisionary surgery. Portal vein embolization (n = 2 patients): Poor results were obtained in these 2 patients. One patient who underwent portal vein embolization alone had overall good results (Terblanche II) after additional revisionary surgery, whereas the second with initial combined portal vein emboli- zation and biliary interventions was listed for liver transplantation because of development of second- ary biliary cirrhosis.Fig 2. Overall results of the revisionary approach. Fullline: Overall results including additional revision. Dotted DISCUSSIONline: Results after ﬁrst-line revision. This study shows that with an experienced multidisciplinary approach (according to the strat- Revision surgery with hepatectomy (n = 4 patients): egy summarized in Fig 3), patients with a failedGood primary results were achieved in 3/4 patients RYHJ after post-cholecystectomy BDI can achievewho were asymptomatic (Terblanche I–II), but the good long-term clinical success in 89%. These re-symptoms did not improve in the other patient. sults required more than the ﬁrst-line revision inThis patient (Terblanche IV) underwent addi- 16% of patients. Although we showed that waitingtional repeat hepatectomy for a bile leak from an for bile duct dilation before revisionary surgery wasexcluded segment 4 with histologic evidence of not successful; moreover, we were unable to iden-secondary biliary cirrhosis, but this procedure tify any prognostic predictive factor at referral infailed. She died from suicide. our small and heterogeneous population. Biliary interventions (n = 16 patients): Good pri- Concordant data suggest that both repair ofmary results were achieved in 14 patients (87%): BDI repair by an expert hepatobiliary surgeon1110 (71%) were asymptomatic (Terblanche I–II) and a multidisciplinary approach involving
6. 100 Benkabbou et al Surgery January 2013Table III. Revisionary surgery procedures (n = 31) Table IV. Percutaneous approach procedures First line Additional (n = 21) (n = 26) (n = 5*) First line Additional (n = 18) (n = 3)Hepaticojejunostomy revision 23 (88%) 4 (80%)Number of ducts/anastomosis Portal vein embolization 2 (11%) 1 1 13 2 Right branch 1 — 2 5 1 Right posterior sector branch 1 1 3 6 — Biliary maneuvers 17 (94%) 3 (100%) 4 1 1 Catheterization approach 5 1 — Transhepatic 9 1Endobiliary extraction 18 (69%) 2 (40%) Transjejunal 4 — Calculi and/or biliary cast 15 2 Combined 4 2 Clips 2 — Endoscopic control 12 (67%) 2 Alimentary 1 1 ProceduresR-en-Y revision with 12 (46%) 0 Stricture dilatation 12 (70%) 3Hepatectomy 4 (15%) 1 (20%) Calculi and/or biliary cast 8 (47%) 1 Right liver 2 — extraction Left liver 2 — Lithotripsy 4 (23%) 1 Left lateral lobe 1 — Suture extraction 2 (12%) —Segment 4 (excluded bile leak) — 1 Median number of procedures 5 (2–23) 10 (2–24)*Second-line in 4 patients and third-line in 1 patient. (range)gastroenterologists, radiologists, and surgeons12favorably affects outcomes. RYHJ has been success- although at the time of initial biliary repair onlyfully used in such cases since the 1970s13 and is cur- 38% of them had an injury or stricture at that level.rently the standard treatment, with success rates Hence, a precise assessment of bile duct anatomyof up to 91% and very long-term (10 years) and the level of the stricture are critical to thestricture-free survival.14,15 Nevertheless, $10% of success of any revisionary strategy.4,16 In this set-these patients will suffer from a failure of the ting, percutaneous cholangiography can be consid-RYHJ.2 ered as the ‘‘gold standard’’ because it provides This failure involves isolated or associated critical information on the biliary anatomy andpathogenic factors responsible for recurrent epi- ductal communication. Magnetic resonance chol-sodes of cholangitis in 90% of patients and/or angiography has been claimed to be as reliable asjaundice in 20%.16 These symptoms of biliary ob- the percutaneous approach in deﬁning biliarystruction may occur without anastomotic stricture tree anatomy20 and may be the procedure ofand are possibly caused by the passage of calculi choice in selected patients.or by enterobiliary reﬂux induced by inappropri- The second major problem encountered in theate construction of the Roux-en-Y limb.2 Between management of RYHJ failure is an absence of intra-80% and 90% of patients with failure of the biliary hepatic bile duct dilation that complicates therepair develop symptoms within 5–7 years.3,17 This biliary repair. This situation was observed in 59%delay can vary from a few days to several years18 (a of our patients. It should be noted that revisionarymaximum of 17 years in our series), which empha- surgery was delayed in 5 patients speciﬁcally to waitsizes the need for prolonged follow-up. By con- for bile duct dilation, but this strategy failed in all 5trast, some patients who are clinically ‘‘normal’’ patients and was associated with severe morbidityafter repair can continue to experience mild during the waiting period. We, therefore, considerincreases in serum bilirubin and/or gamma glu- that when surgical revision criteria are fulﬁlled, antamyl transferase activity during long-term fol- elective procedure assisted by the routine use oflow-up.19 optical magniﬁcation should be scheduled without The management of RYHJ failure is hampered waiting for bile duct dilation.by the fact that biliary strictures are found at a From a technical point of view, if the biliaryhigher level than before the ﬁrst attempt at BDI conﬂuence is intact, a wide stoma of healthy ductrepair. Indeed, with each failed attempt, the level can be achieved by extending the opening in theof the scarred biliary stricture recedes higher into bile duct to the extrahepatic portion of the leftthe hepatic hilum. In our experience, 89% of hepatic duct.21 If the biliary conﬂuence is obliter-referred patients had hilar or suprahilar strictures, ated, and the left and right hepatic ducts are
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