duct injury laparoscopic cholecystectomy: endoscopic … · presence of major bile duct injury in four patients. In general, the clinical presentation of post-operative bile duct

Gut 1993; 34: 1250-1254

Bile duct injury after laparoscopic cholecystectomy:the value of endoscopic retrogradecholangiopancreatography

P H P Davids, J Ringers, E A J Rauws, L Th de Wit, K Huibregtse, M N van der Heyde,G N J Tytgat

AbstractThis study describes the value of endoscopicretrograde cholangiopancreatography (ERCP)in patients with bile duct injury after laparo-scopic cholecystectomy. Twelve consecutivepatients were studied over a one year period.In all patients the biliary tree was visualisedduring ERCP. Four patients had complete bileduct obstruction, seven patients had a stricture(two with concomitant leakage), and onepatient had leakage from a hepatic branch.Three patients with complete obstruction, pre-sented with a relatively prolonged symptomfree, 'silent' period before diagnosis. In all fourpatients with complete transection, a proximalhepaticojejunostomy was performed. In onepatient with a tough fibrous stricture, second-ary to incorrect clip placement, passage of theguidewire was impossible, leaving surgicalreconstruction as the only therapeutic option.All remaining seven patients with leakage orstrictures, or both were successfully treated byendoscopic sphincterotomy only (n=1) orsphincterotomy and subsequent stent place-ment (n=6). When patients do not recoveruneventfully after laparoscopic cholecystec-tomy even without cholestasis or jaundice,early ERCP is recommended as a safe andvaluable method to detect bile duct injury andto suggest treatment. Subsequently, more thanhalf of such patients can be treated endo-scopically. Extended follow up is needed toevaluate the longterm results.(Gut 1993; 34: 1250-1254)

TABLE I Summary ofclinicalfeatures of 12 patients with bile duct injury after laparoscopiccholecystectomy

IntervalCase Agel LC-ERCPNo Sex Presentation (days) ERCP Treatment

1 34/F Cholestasis 17 Stop miid CBD Proximal HJBilomas

2 57/M Sepsis 49 Stop mid CBD HJ, abscess drainage3 21/F Jaundice 27 Stricture mid CBD EBS4 29/F Cholestasis 36 Stricture leakage hilum EBS5 39/F Jaundice 18 Stop mid CBD Proximal HJ

Pain6 38/F Pain, biloma 6 Leakage hepatic branch ES

Cholestasis7 42/M Itching 55 Stricture EBS

Cholestasis8 43/F Cholestasis 70 Stop leakage mid CBD Proximal HJ

Biloma9 33/F Itching 34 Stricture leakage mid CBD EBS

Cholestasis10 45/F Pain 396 Stricture hilum EBS

Cholestasis11 61/M Pain 647 Stricture mid CBD Proximal HJ

Cholestasis12 35/F Nausea 7 Stricture mid CBD EBS

Cholestasis

LC laparoscopic cholecystectomy; HJ hepaticojejunostomy with Roux-en-Y loop;EBS=endoscopic biliary stenting; ES=endoscopic sphincterotomy.

Laparoscopic cholecystectomy has become themost popular method for removing the gallbladder.' 2 Early data suggested that the incid-ence of bile duct injury, which is 1 in 1000 afteropen cholecystectomy," might be 1 in 100 afterlaparoscopic cholecystectomy.3 7 Recent reports,however, show that the incidence may decreaseto 0 30 5% as experience increases.2 8 9

Postoperative bile leakage and benign bileduct stricturing after open cholecystectomy canbe diagnosed safely and effectively with endo-scopic retrograde cholangiopancreatography(ERCP).'° Subsequent endoscopic managementcan be successful in most cases."'16 It has not yetbeen well defined whether a similar approach isjustified for bile duct injury after laparoscopiccholecystectomy. Therefore, we evaluated therole of diagnostic and therapeutic endoscopy in aconsecutive series of patients referred to ourgastroenterology department with bile ductinjury after laparoscopic cholecystectomy.

Patients and methodsBetween May 1991 and June 1992, 12 patients(nine women) were referred for ERCP fromdifferent hospitals, because of suspicion of bileduct injury after laparoscopic removal of the gallbladder. Table I summarises the clinical featuresof these patients. Visualisation of the biliary treewas performed by standard ERCP, with sedationby midazolam given intravenously.'7Our technique and results of endoscopic treat-

ment of bile duct injury after open cholecystec-tomy have been described in detail elsewhere.'3 16In essence our policy is as follows (Table II):when bile duct leakage is present, we prefer todecompress the biliary tree through endoscopicsphincterotomy, often followed by short term(4-6 weeks) insertion of a biliary endoprosthe-sis. When stricturing is present, dilation isattempted by longterm stenting, preferably with

TABLE II Amsterdam treatment protocolfor postoperativebile duct injury

Cholangiography Treatment strategy

Total stop Proximal HJLeakage

Cystic duct stump ESHepatic radical ESCommon bile duct EBSHepatic duct EBSLarge defect EBS

Stone ES and stone extractionStricture EBSLeakage and stricture EBS

HJ=hepaticojejunostomy with Roux-en-Y loop; EBS=endoscopic biliarv stenting; ES=endoscopic sphincterotomv.

Hepatopancreatic-BiliaryUnit, Academic MedicalCentre, University ofAmsterdam, TheNetherlandsP H P DavidsJ RingersE A J RauwsL Th de WitK HuibregtseM N van der HeydeG N J TytgatCorrespondence to:Dr P H P Davids,Hepatopancreatic-Biliary Unit(C2), Academic MedicalCentre, Meibergdreef 9,1105 AZ Amsterdam,The Netherlands.Accepted for publication19 January 1993

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Bile duct injury after laparoscopic cholecystectomy: the value ofendoscopic retrograde cholangiopancreatography

two 10 French gauge (Fg) polyethylene endo-prostheses for one year. These stents areelectively exchanged every three months to avoidclogging induced cholangitis.

Results

CASE 1A 34 year old woman was referred for ERCP, 17days after laparoscopic removal of a shrunkengall bladder, containing one stone. An operativecholangiogram was not performed. Because ofsome peroperative bile leakage, a subhepaticdrain was positioned and antibiotics were givenfor five days. Postoperatively, the patient com-plained of vague abdominal discomfort and thedrain was removed after two days. Bloodchemistry was monitored regularly, but showedonly moderately raised liver enzymes after twoweeks. Abdominal ultrasound imaging showednon-dilated bile ducts, several fluid collections,and guided puncture yielded bile. At ERCP acomplete stop, resulting from a surgical clip atthe level ofthe cystic duct was visualised. Duringlaparotomy, 2 cm ofmore proximal bile duct wasmissing and bile leaked from the commonhepatic duct into the abdominal cavity, explain-ing the absence of obstructive jaundice. Aproximal hepaticojejunostomy with a Roux-en-Yloop reconstruction was performed and thepatient was discharged after three weeks.

CASE 2A 57 year old man was referred for ERCP, 49days after laparoscopic removal of a chronicallyinflamed gall bladder with many adhesions. Anoperative cholangiogram was not performed.Postoperatively, the subhepatic drain produced250 ml bile per day. Unfortunately, the patientinitially refused to have an ERCP. After acci-dental drain removal, the abdomen distendedrapidly and ultrasound showed the presence ofascites. At relaparotomy a large bile duct defectwas seen, located 1-5 cm proximal to the cysticduct and a Roux-en-Y loop was anastomosedover the perforated area. The patient becameseptic and was referred to our intensive care unit.Subsequent ERCP showed a total stop at thelevel of the mid common bile duct (CBD).During the second relaparotomy, multipleabscesses were drained. Eventually, the patientimproved and scintigraphy after one month,showed adequate drainage through the jejunalloop.

CASE 3A 21 year old woman was referred for ERCP, 27days after laparoscopic cholecystectomy. Per-operative cholangiography showed two clipspartially placed over the CBD, which weresubsequently removed. Three weeks after thisprocedure, the patient became jaundiced. Ultra-sound did not show dilated intrahepatic bileducts. At ERCP, a mid CBD stricture at the levelof a clip was detected. Only one 11 cm, 10 Fgstent could be positioned. The jaundice subsidedrapidly and a second stent was inserted after six

Figure 1: Cholangiogram showing total bile duct obstructionbecause oftransverse clip placement over the common bile duct(Case 5).

weeks, to achieve further stretching of thestrictured area.

CASE 4A 29 year old woman was referred for ERCP, 36days after laparoscopic cholecystectomy. Per-operatively, a mid CBD injury was recognisedand the procedure was converted to an opencholecystectomy. The defect was sutured over aT-tube. On the third postoperative day, the T-tube was removed after cholangiography showedsufficient drainage. Three weeks after discharge,the patient felt nauseated and blood chemistryshowed cholestasis. Subsequent ERCP showed asubhilar stricture and some contrast extravasa-tion. Two 14 cm, 10 Fg endoprostheses could beinserted to dilate the stricture. After the pro-cedure the cholestasis subsided.

CASE 5A 38 year old woman was referred for ERCP, 18days after uneventful laparoscopic cholecystec-tomy. After two weeks she became jaundicedand was referred with the diagnosis of choledo-cholithiasis. Subsequent ERCP showed a trans-verse clip over the mid CBD causing a total stop(Fig 1). An attempt to visualise the proximal bile

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Davids, Ringers, Rauws, de Wit, Huibregtse, van der Heyde, Tytgat

ducts resulted in a small perforation. Laparo-tomy showed that the common hepatic duct hadbeen resected erroneously. A cholangiojejuno-stomy with a Roux-en-Y loop was performed,with the left hepatic duct approach.

CASE 6A 39 year old woman was referred for ERCP, sixdays after uneventful laparoscopic cholecystec-tomy. Postoperatively she complained ofabdominal discomfort and blood chemistryshowed cholestasis. Ultrasound showed a smallsubhepatic fluid collection. Subsequent ERCPshowed abundant leakage ofa hepatic radical anda small sphincterotomy was performed tofacilitate bile flow into the duodenum (Fig 2).Possibly a congenital abnormal connection was

present between the cystic duct and the rightbiliary system. The patient improved rapidlyand had no complaints one year after this pro-cedure.

CASE 7

A 42 year old man was referred for ERCP 55days after a complicated laparoscopic chole-cystectomy. Peroperatively bile leakage was

encountered and the procedure was converted toa laparotomy. After CBD exploration a T-tubewas positioned, which was removed after 10days. Nearly two months later the patient com-plained of itching and cholestasis was diagnosed.Abdominal ultrasound showed a stenotic area inthe mid CBD, with prestenotic dilation. Afterfailed ERCP elsewhere, ERCP in our centreconfirmed the presence of a stricture at the levelof a clip. One 14 cm, 10 Fg, stent was positionedand exchanged for two stents after six weeks.

CASE 8A 43 year old woman was referred for ERCP 70days after uneventful laparoscopic removal of a

shrunken gall bladder. Postoperatively, produc-tion from the subhepatic drain diminishedinitially, but after seven days increased to 300to 500 ml bile per day. Ultrasound showed anon-dilated biliary tree and subhepatic fluidcollections. These bilomas were drained per-cutaneously and several attempts at cannulatingthe CBD elsewhere were unsuccessful. Subse-quent ERCP in our institution showed a com-plete disconnection at the level of the mid CBDwith contrast leakage. Despite the non-dilatedbiliary tree, a percutaneous transhepatic cholan-giogram was feasible: there was no communica-tion between the right and the left system andboth branches drained in a subhepatic collection.Laparotomy showed erroneous resection of thetotal hepatic duct confluence. A double cholan-giojejunostomy reconstruction with Roux-en-Yloop was performed with a good result.

CASE 9A 33 year old obese woman was referred forERCP 34 days after uneventful laparoscopicremoval of a chronically inflamed gall bladder,containing one stone. After three weeks shecomplained of itching and blood chemistryshowed cholestasis. At ERCP a mid CBDstricture was visualised at the level of some clips,with concomitant contrast leakage and an endo-prosthesis was inserted. After six weeks, theleakage had stopped and two 10 Fg stents wereinserted.

CASE 10A 45 year old woman was referred 13 monthsafter laparoscopic cholecystectomy. After fivedays, an ERCP elsewhere showed bile leakagefrom the cystic duct stump and a small endo-scopic sphincterotomy was performed, followedby stent insertion. The leakage subsided rapidlyand after three months the stent was removed.Unfortunately, the patient developed pain andcholestasis and a stenosis at the level of the hilumwas diagnosed. Three subsequent balloondilations were unsuccessful and finally thepatient was referred to our institution. DuringERCP a firm stricture, of 3 mm in length, wasvisualised at the level of several clips and onlyone 10 Fg endoprosthesis could be insertedinitially. After six weeks the stricture was furtherdilated with two endoprostheses.

CASE 11A 61 year old man was referred for ERCP nearlytwo years after laparoscopic cholecystectomy.After 35 days he became jaundiced. ERCPelsewhere showed a distal obstructing stone,which was successfully removed with a balloonafter sphincterotomy. In addition, a smallfistulous tract originating from the cystic ductstump was diagnosed. Twenty months later, thepatient again complained of pain in the rightupper abdomen. Blood chemistry showed recur-rent cholestasis. Subsequent ERCP showed avery tight mid CBD stricture at the level ofseveral clips (Fig 3). During two consecutiveattempts, passage of a guidewire was impossible.

Figure 2: Cholangiogramshowing abundant bileleakagefrom a secondaryright hepatic branch (arrow),which stopped after a smallsphincterotomy (Case 6).

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Bile duct injury after laparoscopic cholecystectomy: the value ofendoscopic retrograde cholangiopancreatography

Figure 3: Firm mid common bile duct stricture (arrow), twoyears after laparoscopic cholecystectomy. Although theproximal biliary tree could be visualised, guidewire passagewas impossible during two attempts (Case 11).

After these manipulations, one clip migratedinto the CBD and was successfully removed witha Dormia catheter. Later on a hepaticojejuno-stomy was performed with good result.

CASE 12A 35 year old woman was referred for ERCPseven days after uneventful laparoscopic chole-cystectomy. Three days postoperatively she feltnauseated. Blood chemistry showed cholestaticliver enzymes and ultrasound showed dilatedbile ducts. At ERCP a subhilar stricture was

visualised with surrouding clips and one 14 cm,

Figure 4: Left: Subhilarstricture because ofa clip(arrow). Right: One 10 Fg,14 cm stent was inserted andexchangedfor two stentsafter six weeks (Case 12).

10 Fg stent was inserted successfully (Fig 4). Asecond stent was positioned after six weeks.

DiscussionIn all the 12 patients referred with suspicion ofbile duct injury, the biliary tree was successfullyvisualised during ERCP. This led to a furtherdiagnosis and aided treatment strategy. Remark-ably, previous abdominal ultrasound showednon-dilated intrahepatic bile ducts despite thepresence of major bile duct injury in fourpatients.

In general, the clinical presentation of post-operative bile duct injury includes distinctsymptoms such as cholestasis, jaundice, persist-ent bile drainage by drains and sepsis as des-cribed after open cholecystectomy.18 Moreimportant, however, is the occasional presenceof an initial relatively symptom free period,which can mislead the clinician. In this study,three patients (cases 1, 5, and 8) with completebile duct transection had indeed initially little, ifany, complaints. This symptom free periodlasted for several days and even weeks. After thisclinically 'silent' period, the patients eventuallydeveloped cholestasis. Surprisingly, subsequentERCP showed a complete bile duct obstruction.In all three patients, subsequent laparotomyshowed a distal CBD occluded by clips and apartially resected common hepatic duct, withfree bile leakage into the abdominal cavity.Unhindered bile flow from the liver, may explainthis initial 'silent', anicteric period.

According to our experience, the severity ofbile duct injuries seems to be changed afterlaparoscopic cholecystectomy. For the lastdecade, about one patient a year was referred toour department with a total bile duct transectionafter open cholecystectomy."6 In contrast, afterthe introduction of the laparoscopic approach,four patients have been referred with total bileduct transections during a one year period.Important factors that may contribute to thisapparently increased incidence ofmajor bile ductinjuries after laparoscopic cholecystectomy, areabsence of three dimensional depth perceptionduring laparoscopy, a changed view on theoperative field, and tenting of the common bileduct by anterior traction on the gall bladder todissect Calot's triangle.'920 In general, a largeproportion of bile duct injuries can be attributedto the learning experience of the surgeon.2

All four patients with complete bile ducttransection were treated with a proximal hepati-cojejunostomy with Roux-en-Y jejunal loop.When the total common hepatic duct wasresected, the left hepatic duct approach was usedfor the hepaticojejunal anastomosis.2' It wasdifficult to perform a suficiently wide bilio-enteric anastomosis in two of four patients,because of a non-dilated biliary tree. Whetherthis will influence the longterm patency of theanastomosis, remains to be seen.The treatment of bile leakage after open

cholecystectomy, by endoscopic sphincterotomyor stent placement has been reported -to yieldacceptable results, especially when the patient isreferred in an early phase.'322 In this study, allthree patients with bile leakage were also suc-

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cessfully treated endoscopically. This shows thatsimilar guidelines for decompression of thebiliary tree after open cholecystectomy, can beapplied after laparoscopic cholecystectomy aswell.The role of endoscopic stenting for postopera-

tive biliary strictures is still debated.23 We haveadvocated initial endoscopic stenting for bileduct strictures after open cholecystectomy.24 Bileduct stricturing after laparoscopic cholecystec-tomy is often due to clip mis or displacement.When these strictures are temporarily dilated byendoscopic stenting, the permanent presence ofthese clips might perhaps induce restricturingafter stent removal. Nevertheless, a proximalhepaticojejunostomy in a young patient seemsunattractive and justifies exploration of other,less invasive, alternatives. Moreover, in case ofendoscopic failure surgical options are still avail-able.

Six of seven patients with a stricture, hadsuccessful stent insertion. Extended follow up isrequired, to assess the longterm effects, particu-larly the stricture recurrence rate after final stentremoval. In one patient, who presented with astricture nearly two years after laparoscopiccholecystectomy, surgery seemed to be the onlyoption. Even after transpapillary removal of oneclip, guidewire passage remained impossible.Occasionally, however, stent placement canbecome feasible after endoscopic clip removal.25

Intraoperative cholangiography, performed inonly one patient in this study, can be helpful indelineating the biliary anatomy to avoid iatro-genic injury.2627 Possibly, selected or routine useof intraoperative cholangiography could haveprevented or diagnosed some of the injuries.When bile duct injury is diagnosed, optimal

management can only be achieved by a team,including surgeon, endoscopist, and radio-logist.28 This study has shown that cliniciansmust be aware of the occasional 'silent' periodafter major bile duct injuries. Whenever patientsdo not recover uneventfully after laparoscopiccholecystectomy, early ERCP is a safe andvaluable approach to visualise the location andextent of any lesion. More than half of suchpatients can be treated endoscopically.

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13 Davids PHP, Rauws EAJ, Tytgat GNJ, Huibregtse K.Postoperative bile leakage: Endoscopic management. Gut1992;33: 1118-22.

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24 Davids PHP, Tanka AJF, Rauws EAJ, et al. Benign biliarystrictures: Surgery or Endoscopy? Ann Surg 1993; 217:237-43.

25 Weber J, Adamek HE, Riemann JF. Endoscopic stent place-ment and clip removal for common bile duct stricture afterlaparoscopic cholecytectomy. Gastrointest Endosc 1992; 38:181-2.

26 Berci GB, Sackier JM, Paz-Partlow M. Routine or selectedintraoperative cholangiography during laparoscopiccholecystectomy? Am] Surg 1991; 161: 355-60.

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