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OLTX for Bile Duct Injury 355

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Tohoku J. Exp. Med., 2006, 209, 355-359

Received March 22, 2006; revision accepted for publication May 15, 2006.Correspondence: Koray Acarlı, Valikonağı Caddesi, Polat Apartmanı 169/6, Nisantası, 34365, İstanbul,

Turkey.e-mail: [email protected]

Case Report

Bile Duct Injury during Cholecystectomy Requiring Delayed Liver Transplantation: A Case Report and Literature Review

DIDEM ÖNCEL, İLGIN ÖZDEN, ORHAN BILGE, YAMAN TEKANT, KORAY ACARLI, AYDIN ALPER, ALI EMRE and ORHAN ARIOĞUL

Department of General Surgery (Hepatopancreatobiliary Surgery Unit), Istanbul University, Istanbul Faculty of Medicine, Istanbul, Turkey

ÖNCEL, D., ÖZDEN, İ, BILGE, O., TEKANT, Y., ACARLI, K., ALPER, A., EMRE, A. and ARIOĞUL, O. Bile Duct Injury during Cholecystectomy Requiring Delayed Liver Trans-plantation: A Case Report and Literature Review. Tohoku J. Exp. Med., 2006, 209 (4), 355-359 ── Major bile duct injury during cholecystectomy represents potentially severe complications with unpredictable long-term results. If these lesions are not treated ade-quately, they can lead to hepatic failure or secondary biliary cirrhosis therefore requiring liver transplantation. We report a patient who required liver transplantation 15 years after open cholecystectomy. A l0-year old girl underwent open cholecystectomy and duodenal repair for cholelithiasis and cholecystoduodenal fistula. She required two surgical inteven-tions, hepaticojejunostomy which was performed in another center and portoenterostomy for biliary stricture at our institution seven years after the cholecystectomy. Eight years after the third operation, she required recurrent hospitalization for treatment of hepatic abscesses. The extremely short intervals between the three life threatening epi-sodes and the rapid progression to severe sepsis were taken into consideration and liver transplantation was performed at the age of 25. She is leading a healthy life at 4 years post transplantation. Although iatrogenic biliary injury can usually be treated successfully by a combination of surgery, radiological and endoscopic techniques, patients with severe inju-ries develop irreversible liver disease. This case report and review of the literature suggest that liver transplantation is a treatment modality for a selected group of patients with end-stage liver disease secondary to bile duct injury. ──── bile duct injury; secondary biliary cirrhosis; liver transplantation© 2006 Tohoku University Medical Press

Biliary and hepatic vascular injuries during cholecystectomy are complex lesions, associated with high rates of morbidity and mortality (Lillemoe et al. 1997; Buell et al. 2002). The incidence of major bile duct injury has remained

constant at the rate of 0.1-0.3% during open sur-gery, and 0.3-1% during laparoscopic surgery. Although some centers report successful results in almost all patients with a combination of surgery and radiological techniques (Lillemoe et al. 1997;

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Johnson et al. 2000), biliary cirrhosis cannot always be prevented (Nordin et al. 2001). An associated vascular injury may occur in 10-30% of these patients, and although it generally remains “silent,” in rare cases it may lead to extensive hepatic necrosis (Bacha et al. 1994; Erkan et al. 2001; Nordin et al. 2001). These are the two serious complications of a benign disease that may eventually require liver transplantation. In this paper, we present a case of bile duct injury following open cholecystectomy, which resulted in secondary biliary cirrhosis requiring liver trans-plantation and also review the world literature.

CASE REPORT

A 10-year old girl underwent open cholecys-tectomy at other institution in 1987. At laparoto-my, the gallbladder was found to be fistulized to the duodenum, and cholecystectomy and duode-nal repair were performed. The postoperative period was complicated with both biliary and duodenal fistulae. The biliary fistula was treated by a Roux-en-Y hepaticojejunostomy (HJS), whereas the duodenal fistula was treated conser-vatively. This second operation showed a definite biliary tract injury, with no signs of any congeni-tal abnormality.

Seven years later, she was referred to our institution, for recurrent cholangitis. She was fol-lowed conservatively for one year but her clinical course warranted an intervention. Her percutane-ous transhepatic cholangiography (PTC) revealed a Bismuth III stricture. Preoperative color Doppler ultrasound showed normal flow pattern in both the portal vein and hepatic arteries. During exploratory laparotomy, which was done seven years after her first operation, the HJS was found to be stenosed, and surrounded by dense, fibrotic tissues. Although the preoperative surgi-cal strategy was to perform a HJS alone or fol-lowing extended hepatectomy, attempts to find healthy bile ducts suitable for anastomosis were unsuccessful and a portoenterostomy (similar to

A

B

Fig. 2. T2-weighted Magnetic Resonance Imaging showing hepatic abscess in segment 7. The abscess is marked with arrows.

Fig. 1. Percutaneous transhepatic cholangiography. A: Complex biliary strictures in the hepatic hilus. B: Balloon dilation of the strictures. The strictured and dilated segments are marked with arrows.

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the Kasai procedure) was performed. An intraop-erative liver biopsy confirmed presence of biliary cirrhosis. She was started on ursodeoxycholic acid treatment. Except for self-limiting or mild episodes of cholangitis, her bilirubin level remained below 2 mg/dl for six years until June 2000, when the total bilirubin level rose to 4.2 mg/dl and did not become lower than 2.7 mg/dl until October 2000. Her ultrasonographic evalua-tion showed dilation of the intrahepatic biliary tree. PTC and balloon dilation of the hilar stric-tures were performed (Fig. l A and B). Her biliru-bin level gradually decreased to l.4 mg/dl by May 2001. However, between October 2001 and February 2002, she was hospitalized three times for severe sepsis due to hepatic abscesses in the right lobe (Fig. 2). She underwent percutaneous drainage and required admission to the intensive care unit. Radiological examinations performed at that time did not show significant dilation of the biliary tree, therefore PTC and balloon dila-tion were not attempted. Given the extremely short intervals between the three life threatening episodes and the rapid progression from prodro-mal symptoms to severe sepsis, it was decided to perform a liver transplantation. Her preoperative liver function tests were as follows: total biliru-bin, 4.7 mg/dl; aspartate aminotransferase 47 U/L; alanine aminotransferase 42 U/L; alkaline phos-phatase 478 U/L; albumin 3.0 g/dl; and prothrom-bin time 16 seconds. The Magnetic Resonance Imaging showed signs of cirrhotic liver, left hepatic lobe atrophy and dilation of the intrahe-patic bile ducts. After obtaining informed con-sent, orthotopic liver transplantation from a blood group identical donor was performed. At opera-tion, the hepatic artery and its branches were found to be intact. Her postoperative course was uneventful. The pathologic findings were consis-tent with inactive cirrhosis. She is leading a healthy life at 4 years post transplantation.

DISCUSSION

The hepatic vasculature and the biliary tree may be injured during cholecystectomy (Lillemoe et al. 1997; Nishio et al. 1999; Erkan et al. 2001; Koffron et al. 2001; Buell et al. 2002; Bilge et al.

2003). Although bile duct injury is more com-mon, detailed studies show that “silent” concomi-tant arterial injury may be detected in patients with bile duct injury (Erkan et al. 2001; Koffron et al. 2001; Nordin et al. 2001). In rare cases, vascular injury occurs alone and causes dramatic tissue damage that initiates a series of events that lead to liver transplantation. The first report on such a patient was published in 1994. Inadvertent clipping of the right hepatic artery resulted in the development of a hepatic abscess in the right lobe and “necrosis in the central bile ducts” (Bacha et al. 1994). In the absence of extensive hepatic infarction due to vascular injury, the liver can usually be salvaged by treatment of the biliary lesion. However, since 1994, reports of patients who required liver transplantation for secondary biliary cirrhosis due to biliary tract injury (with and without concomitant vascular injury) have been published (Bacha et al. 1994; Robertson et al. 1998; Loinaz et al. 2001; Nordin et al. 2001, 2002; de Santibanes et al. 2002; Fernandez et al. 2004) (Table1).

Surgery is the main treatment method for complex biliary injuries. Unfortunately, a sub-group of patients (0-19%) has less than satisfacto-ry outcome during a mean follow-up of only 12-36 months (Ahrendt and Pitt 2001). The data on the long-term outcome of these patients are sparse. Although some centers report successful results in almost all patients with a combination of surgery and radiological techniques (Lillemoe et al. 1997; Johnson et al. 2000), biliary cirrhosis cannot always be prevented (Nordin et al. 2001). It must be noted that the patient reported in this paper had to undergo transplantation 15 years af-ter cholecystectomy.

Roux-en-Y HJS is the technique of choice in the management of bile duct injuries occurring during open or laparoscopic surgery. Never-theless, it is a technically demanding operation, which can ultimately lead to secondary biliary cir-rhosis, especially if it fails in the first attempt (Mirza et al. 1997; Nordin et al. 2002; Fernandez et al. 2004). One possible cause of reconstruction failure may be concomitant vascular injury, which is clinically silent in the majority of the patients

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(Bilge et al. 2003). Although some reports accept concomitant vascular injury as a significant prog-nostic indicator, autopsy findings and anatomical studies do not support this idea. The authors do not recommend routine angiography since an association between vascular injuries and clinical outcome has not been shown (Bilge et al. 2003).

It must also be stressed that in many papers, outcome is rated as excellent “if there were no symptoms attributable to the biliary tract injury or reconstruction” or good “if mild symptoms not requiring invasive investigation and treatment” (Lillemoe et al.1997; Ahrendt et al. 2001). In other words, these “success” definitions include patients with residual cholestasis that has been asymptomatic during follow up. The long-term fate of the patients without excellent results according to the criteria proposed by Schweizer et al. (1991) (normal alkaline phosphatase, freedom from cholangitis, no obstruction and/or calculi on radiological investigations) has not received adequate attention. This issue is particularly important because the mean age of the patients with biliary injury is in the 40-50 ranges, i.e., a patient group with long life expectancy (Lillemoe et al. 1997; Johnson et al. 2000; Loinaz et al. 2001; Buell et al. 2002). This case report and review of the literature suggests that liver trans-

plantation will be a treatment modality for a selected group of patients with end-stage liver disease secondary to bile duct injury.

ReferencesAhrendt, S.A. & Pitt, H.A. (2001) Surgical therapy of iatrogen-

ic lesions of biliary tract. World J. Surg., 25, 1360-1365.Bacha, E.A., Stieber, A.C., Galloway, J.R. & Hunter, J.G. (1994)

Nonbiliary complication of laparoscopic cholecystectomy. Lancet, 344, 896-897.

Bilge, O., Bozkıran, S., Özden, İ., Tekant, Y., Acarlı, K., Alper, A., Emre, A. & Arıoğul, O. (2003) The effect of concomi-tant vascular disruption in patients with iatrogenic biliary injuries. Langenbecks Arch. Surg., 388, 265-269.

Buell, J.F., Cronin, D.C., Funaki, B., Koffron, A., Yoshida, A., Lo, A., Leef, J. & Millis, J.M. (2002) Devastating and fatal complications associated with combined vascular and bile duct injuries during cholecystectomy. Arch. Surg., 137, 703-710.

de Santibanes, E., Pekolj, J., McCormack, L., Nefa, J., Mattera, J., Sivori, J., Bonofiglio, C., Gadano, A. & Ciardullo, M. (2002) Liver transplantation for the sequelae of intra-operative bile duct injury. HPB, 4, 111-115.

Erkan, M., Acarli, K., Ozden, I., Emre, A., Alper, A., Bilge, O., Tekant, Y. & Ariogul, O. (2001) Negative prognostic factors in iatrogenic bile duct injuries. 4th Congress of the European Chapter of the International Hepato-Pancreato-Biliary Association, Amsterdam, p. 34.

Fernandez, J.A., Robles, R., Marin, C., Sanchez-Bueno, F., Ramirez, P. & Parrilla, P. (2004) Laparoscopic iatrogeny of the hepatic hilum as an indication for liver transplantation. Liver Transpl., 10, 147-152.

Johnson, S.R., Koehler, A., Pennington, L.K. & Hanta, D.W. (2000) Long-term results of surgical repair of bile duct injuries following laparoscopic cholecystectomy. Surgery, 128, 668-677.

TABLE 1. Previous reports on bile duct and hepatic vascular injuries associated with cholecystectomy that required liver transplantation.

Author Year Numberof cases Type of surgery Primary intervention

Type of injury

Biliary Vascular

Bacha et al. 1994 1 LC Right lobectomy 0 1Robertson et al. 1998 1 LC HJS 1 1Nordin et al. 2001 4 3 LC, 1OC 3 HJS, 1 Revascularization 4 1Loinaz et al. 2001 4 OC ? 4 ?Nordin et al. 2002 1* LC None 1 1De Santibanes et al. 2002 5 3 LC, 2 OC 2 HJS, 3 EEA-T tube 5 1Fernandez et al. 2004 3 LC 1 HJS, 2 Hemostasis 3 2This case 2006 1 OC HJS 1 0

LC, laparoscopic cholecystectomy; OC, open cholecystectomy; HJS, hepaticojejunostomy; EEA, end-to-end anastomosis.

* This report also contained the three patients that were published in 2001, which were excluded from this table, to prevent double count.

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Koffron, A., Ferrario, M., Parsons, W., Nemcek, A., Saker, M. & Abecassis, M. (2001) Failed primary management of iat-rogenic biliary injury: incidence and significance of con-comitant hepatic arterial disruption. Surgery, 130, 722-731.

Lillemoe, K., Martin, S.A., Cameron, J.L., Yeo, C.J., Talamini, M.A., Kaushal, S., Coleman, J., Venbrux, A.C., Savader, S.J., Osterman, F.A. & Pitt, H.A. (1997) Major bile duct injuries during laparoscopic cholecystectomy: Follow-up after combined surgical and radiologic management. Ann. Surg., 225, 459-471.

Loinaz, C., Gonzales, E.M., Jimenez, C., Garcia, I., Gomez, R., Gonzales-Pinto, I., Colina, F. & Gimeno, A. (2001) Long-term biliary complications after liver surgery leading to liver transplantation. World J. Surg., 25, 1260-1263.

Mirza, D.F., Narsimhan, K.L., Ferraz Neto, B.H., Mayer, A.D., McMaster, P. & Buckels, J.A. (1997) Bile duct injury fol-lowing laparoscopic cholecystectomy: referral pattern and management. Br. J. Surg., 84, 786-790.

Nishio, H., Kamiya, J., Nagino, M., Uesaka, K., Kanai, M., Sano, T., Hiramatsu, K. & Nimura, Y. (1999) Right hepatic

lobectomy for bile duct injury associated with major vascular occlusion after laparoscopic cholecystectomy. J. Hepatobiliary Pancreat. Surg., 6, 427-430.

Nordin, A., Makisalo, H., Isoniemi, H., Halme, L., Lindgren, L. & Hockerstedt, K. (2001) Iatrogenic lesion at cholecystec-tomy resulting in liver transplantation. Transplant. Proc., 33, 2499-2500.

Nordin, A., Halme, L., Makisalo, H., Isoniemi, H. & Hockerstedt, K. (2002) Management and outcome of major bile duct injuries after laparoscopic cholecystectomy: from therapeutic endoscopy to liver transplantation. Liver Transpl., 8, 1036-1043.

Robertson, A.J., Rela, M., Karani, J., Steger, A.C., Benjamin, I.S. & Heaton, N.D. (1998) Laparoscopic cholecystectomy injury: an unusual indication for liver transplantation. Transpl. Int., 11, 449-451.

Schweizer, W.P., Matthews, J.B., Baer, H.U., Triller, J., Halter, F., Gertsch, P. & Blumgart, L.H. (1991) Combined surgical and radiological approach for complex benign biliary tract obstruction. Br. J. Surg., 78, 559-563.