SciELO - Scientific Electronic Library Online

vol.37 issue6Assessment of positive perioperative cholangiography in patients undergoing elective laparoscopic cholecystectomyPancreatic heterotopias: clinicopathological analysis of 18 patients author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand




Related links


Revista do Colégio Brasileiro de Cirurgiões

Print version ISSN 0100-6991

Rev. Col. Bras. Cir. vol.37 no.6 Rio de Janeiro Nov./Dec. 2010 



The influence of time referral in the treatment of iatrogenic lesions of biliary tract 



Fernando Barros, ACBC-RJI; Reinaldo Afonso FernandesII; Marcelo Enne de Oliveira, TCBC-RJIII; Lúcio Filgueiras PachecoIV; José Manoel da Silva G. Martinho, TCBC-RJV

ISurgeon, Hospital Universitário Antônio Pedro. Master's Degree in General Surgery, Universidade Federal Fluminense
IIMember, Liver Transplantation Team, Hospital Geral de Bonsucesso - Rio de Janeiro - Brazil
IIIMember, Liver Transplantation Team, Hospital Geral de Bonsucesso. Master's Degree in General Surgery, Universidade Federal do Rio de Janeiro
IVHead, Hepato-Biliary Surgery and Liver Transplantation, Hospital Geral de Bonsucesso. Master's Degree in General Surgery, Universidade Federal do Rio de Janeiro
VMember, Liver Transplantation Team, Hospital Geral de Bonsucesso. Master's Degree in Gastroenterology Surgery and PhD in General Surgery, Universidade Federal do Rio de Janeiro

Address for correspondence




OBJECTIVE: To evaluate the prognosis of patients with iatrogenic bile duct injury (IBDI) regarding time of referral (RT) to the unit of liver transplantation (LT).
METHODS: We reviewed 51 charts of patients who had suffered some kind of IBDI during cholecystectomy and who were referred to the Bonsucesso General Hospital (HGB) LT unit. Lesions were grouped according to the Bismuth classification. Besides cholecystectomy (time of injury), we also evaluated the RT and outcome.
RESULTS: Among the 51 patients studied, there were 17 men and 34 women, with a mean age of 42.7 years. Twenty-two patients (43.1%) had a type II lesion, 13 (25.5%) type III, 10 (19.6%) type I, 5 (9.8%) type IV and only 1 (2%) type V. Forty patients were operated, and three did not return for medical review, therefore, 37 were evaluated in relation to outcome. Among these, 25 patients (67.6%) had excellent or good results with average RT of 11.5 months (range: 2-48 months) and 47.2 months (range: 3-180 months) respectively. The 12 patients (32.4%) with poor results had a mean RT of 65.9 months (range: 3 264 months), which was significantly higher than the group with excellent or good results (p=0.004). Seven patients were listed for LT, but only two were transplanted. The RT of these seven patients was significantly higher (p=0.04) than those patients not listed. Seven patients died, six of which were due to liver complications. Conclusion: RT significantly influenced the prognosis of patients in our sample.

Key words: Cholecystectomy/adverse effects. Hepatic cirrhosis. Biliary ducts/lesions.  Iatrogenic disease. Post-operative complications.




More than 750,000 cholecystectomies are carried out annually in the United States of America, one of the most largely performed gastrointestinal surgeries1. Over 80% of benign biliary strictures (BBS) occur as a complication of cholecystectomy. The incidence of iatrogenic bile duct injuries (IBDI) has increased since the advent of laparoscopy in the late 1980s. The BBS is still a problem today, almost 20 years after the recognition of laparoscopy as the gold standard in the treatment of biliary lithiasis. This was very clear at the joint meeting of the Society of American Gastrointestinal Endoscopic Surgeons (SAGES) and the American Hepato-Biliary-Pancreatic Association held in April 20052. On that occasion, more than 300 surgeons discussed various topics surrounding the IBDI, highlighting the increase in incidence in the laparoscopic era (from 0.1 to 0.3% to 0.4-0.6%).

Some risk factors for IBDI are well documented, such as inflammation of the gallbladder3-5, anatomic variations6, learning curve7-10, poor technique employed11 and the non performance of intraoperative cholangiography or other image method12-14.

The IBDI can have serious complications if not properly and timely treated. Patients may experience repeated episodes of cholangitis, biliary cirrhosis (HBC), liver failure and death. Some variables have been proposed to explain the different results of treatment between these patients: the level of estenosis15, extent and quality of the proximal bile duct16, the number of previous attempts to repair it17,18, hepatic function19, laparoscopic versus conventional cholecystectomy20,21,22, diagnosis of the injury still during surgery16,23 and especially the experience of the multidisciplinary team to deal with te problem24,25. However, the time between injury and surgical repair by a team of liver transplantation (LT) in a tertiary center (reference time - RT), has not been described as a modifying factor in these patients' outcome.



We analyzed medical records of 51 patients with IBDI referred to the Liver Transplant Service of Bonsucesso General Hospital from September 1999 to September 2009. Only patients with BBS were included. Patients who underwent biliary-enteric bypass due to other causes (stones, post-transplant, choledochal cyst, trauma or tumors) were excluded from the analysis. Of the 51 patients, 40 were operated until the end of this work. However, three did not return for review and could not enter the analysis of outcome.

The BBS were grouped according to the Bismuth classification26. Patients were contacted by telephone, telegram or e mail and asked to return to the unit for monitoring. The information on cholecystectomy and RT were gathered to complete the medical reports. During the clinical examination, patients were asked about the presence of symptoms suggestive of cholestasis, such as fever, chills, rash, abdominal pain and discharge of bile from the wound. Aiming to further elucidate the complaints we requested laboratory tests (complete blood count, transaminases, bilirubin and fractions, alkaline phosphatase, gamma-GT) and an ultrasound to evaluate the biliary tract.

Treatment outcomes were classified based on clinical and laboratory examination: 1) excellent, if the patient remained completely asymptomatic with normal or stable levels of liver enzymes; 2) good, if the patient presented with symptoms without the need for hospital or residential treatment or only one episode of cholangitis, but without the need for surgery, 3) poor, if subjected to two or more episodes of cholangitis, need for surgery, progression to HBC and therefore listed for LT27.

The software SPSS for Windows (SPSS Inc., Chicago, IL, USA) was used for data analysis and statistical comparisons. The analysis of RT and outcome was performed using the Kruskal-Wallis nonparametric test and, additionally, the Mann-Whitney test. A p value <0.05 was considered significant for all tests.



As shown in Table 1, our sample comprised 34 women and 17 men with a mean age of 42.7 years (range: 3-71); 30 were Caucasians, 14 mulattoes and seven African Brazilian. Thirty-five patients (68.6%) came from hospitals with residency program in general surgery. Forty patients were operated. Another 11 patients were treated conservatively (five cases) or are still awaiting the best time for surgical approach (six cases). Three patients did not continue the treatment. The mean follow up was 44.6 months (range: 5-117).

According to the Bismuth classification, the type II lesion was the most common (22 patients, 43.1%), followed by type III (13 patients, 25.5%), type I (10 patients, 19.6% ), type IV (five patients, 9.8%) and type V (one patient, 2.0%). One patient who had type IV also had an associated vascular injury (left portal vein). With respect to cholecystectomy, we found 27 patients (52.9%) who suffered the injury during elective surgery, 16 of these by conventional surgery and 11 by laparoscopy. Twenty-four patients (47.1%) were operated on an emergency basis, 15 cases by conventional surgery and nine by laparoscopy. We found no significant difference between patients operated by laparoscopic vs. conventional surgery (p=0.564).

The Hepp-Couinaud Surgery was the choice of treatment whenever possible (26 cases, 51%) (Table 1). The second most frequent was the Roux-en-Y hepaticojejunostomy (nine cases, 17.6%), followed by left hepatectomy with right hepaticojejunostomy (two cases, 3.9%) and only one case (2%) of coledocojejunostomy, "T" tube biliary drainage and external drainage of the cavity due to inability to visualize the bile duct. Nine surgeries (17.6%) had to be carried out urgently (eight cases of cholangitis and one of choleperitoneum). Twenty-seven anastomoses (67.5%) were made using a running, single plane, 6.0, PDS suture. A closed tubular drain was used to drain the cavity for an average of 6.5 days (range: 4 18). Seven patients (12.5%) complicated with biliary fistula and one (2%) with enteric fistula, all resolved with supportive care. The average duration of postoperative hospitalization was 15.5 days (range: 5-90). Until the outcome of this study, there was no need for any new operation.


Among the operated patients, 25 (67.6%) were classified as having an excellent or good outcome whilst 12 (32.4%) had a poor one. The average RT for patients with poor, good and excellent results was, respectively, 65.9 months (range: 3-264 months), 47.2 months (range: 3-180 months) and 11.5 months (range: 2 -48 months), respectively (Figure 1), with statistical significance (p=0.004). Pairwise comparisons between these groups also showed that patients with excellent results had a significantly lower RT than those with good results (p=0.007) and poor results (p=0.004).



Six patients were listed for Liver Transplantation; their mean RT was 84.5 months (range: 3-264 months). This time was significantly longer (p=0.04) when compared with patients who were not listed (average of 27.9 months, range 2-180 months) (Figure 2). One patient was transplanted (cadaveric donor), but died on the 14th postoperative day (RT = 96 months) due to liver failure. A total of seven patients died due to: encephalopathy (two cases), upper gastrointestinal bleeding (two cases), liver failure (one case), biliary sepsis (one case) and acute myocardial infarction (one case).




Several methods are accepted in the current literature for the treatment of IBDI. The procedures include everything from an esophageal stent by endoscopy up to complex derivative operations. Currently, there are numerous ways to make a bypass through a biliodigestive anastomosis. However, due to the variety of injuries that can be found, choosing the appropriate operation for each patient can be crucial for outcome. Most authors agree that the best method for treating IBDI is through a biliary-enteric Roux-Y bypass, as shown by Lillemoe et al.25. All patients with complete section of the biliary tract treated with primary anastomosis and biliary "T" drain had a poor prognosis. In contrast, the success rate was 63% among those in whom surgical repair was the Roux-Y bypass. In our sample, the Hepp-Couinaud surgery was preferred when the left hepatic duct was good and when the hepatic duct confluence was intact, as suggested by other authors20. By the end of the study, no patient had returned with restenosis.

In two cases a left hepatectomy combined with a right hepaticojejunostomy was necessary due to HBC. Although these two patients did not require further intervention, one had serious septic complications of biliary origin. However, Santibañes et al.20 reported good results for IBDI patients who required hepatectomy.

It is unclear in the literature whether the RT to a tertiary center with a team with experience in LT may influence outcome. The average RT for the 37 patients who underwent surgery and returned for review was 38.8 months (range: 2-264 months). Patients with poor results had a higher RT compared to those with excellent or good results (p=0.004). Patients with a short RT had a smaller number of previous surgeries, better results and were less frequently listed for transplant.

Although the short-term consequences of IBDI are significant, it is the long-term outcome that will determine the success of surgical treatment. The largest series of follow-up of patients treated surgically was presented by Lillimoe et al.25. Of the 156 patients with BBS who underwent surgery, 142 completed treatment with a mean follow up of 57.5 months. Of these, 90.8% were considered to have excellent or good results. The mean follow up of our 37 patients was 44.9 months (range: 2-117 months). Twenty-five (67.5%) of them were classified as having excellent or good results.

Some authors suggest that different mechanisms of the laparoscopy injury, its complex nature and the frequent association of inflammation and fibrosis secondary to undiagnosed small fistulas can worsen prognosis17,22. Nevertheless, we found no significant difference between patients who sustained the injury during an operation by laparoscopy or conventional surgery (p=0.564). Therefore, the excellent results reported in some studies of patients treated with conventional surgery should be interpreted with caution17, 22.



1. Graves EJ, Owings MF. National Hospital Discharge Survey. Advance data from vital and health statistics 1997;no. 291. National Center of Health Statistics.         [ Links ]

2. Larso GM. Laparoscopic biliary tract injury: what are the limits of prevention? [editorial] Surg Endosc. 2006;20911):1635-7.         [ Links ]

3. Deziel DJ, Millikan KW, Economou SG, Doolas A, Ko ST, Airan MC. Complications of laparoscopic cholecystectomy: a national survey of 4,292 hospitals and an analysis of 77,604 cases. Am J Surg. 1993;165(1):9-14.         [ Links ]

4. Pitt HA, Miyamoto T, Parapatis SK, Tompkins RK, Longmire WP Jr. Factors influencing outcome in patients with postoperative biliary strictures. Am J Surg. 1982;144(1):14-21.         [ Links ]

5. Wherry DC, Marohn MR, Malanoski MP. An external audit of laparoscopic cholecystectomy in the steady state performed in medical treatment facilities of the department of defense. Ann Surg. 1996;224(2):145-54.         [ Links ]

6. Kurumi Y, Tani T, Hanasawa K, Kodama M. The prevention of bile duct injury during laparoscopic cholecystectomy from the point of view of anatomic variation. Surg Laparosc Endosc Percutan Tech. 2000;10(4):192-9.         [ Links ]

7. Cohen MM, Young W, Theriault ME. Has laparoscopic cholecystectomy changed patterns of practice and patient outcome in Ontario? CMAJ. 1996;154(4):491-500.         [ Links ]

8. Russell JC, Walsh SJ, Mattie AS, Lynch JT. Bile duct injuries, 1989-1993. A statewide experience. Connecticut Laparoscopic Cholecystectomy Registry. Arch Surg 1996;131(4):382-8.         [ Links ]

9. Windsor JA, Pong J. Laparoscopic biliary injury: more than a learning curve problem. Aust N Z J Surg 1998;68(3):186-9.         [ Links ]

10. Tantia O, Jain M, Khanna S, Sen B. Iatrogenic biliary injury: 13,305 cholecystectomies experienced by a single surgical team over more than 13 years. Surg Endosc. 2008;22(4):1077-86. Epub 2008 Jan 18.         [ Links ]

11. Callery MP. Avoiding biliary injury during laparoscopic cholecystectomy: technical considerations. Surg Endosc. 2006;20(11):1654-8 Epub 2006 Oct 24.         [ Links ]

12. Traverso LW. Intraoperative cholangiography lowers the risk of bile duct injury during cholecystectomy. Surg Endosc. 2006;20(11):1659-61. Epub 2006 Oct 23.         [ Links ]

13. Sarli L, Costi R, Roncoroni L. Intraoperative cholangiography and bile duct injury. Surg Endosc. 2006;20(1):176-7. Epub 2005 Dec 7.         [ Links ]

14. Machi J, Johnson JO, Deziel DJ, Soper NJ, Berber E, Siperstein A, et al. The routine use of laparoscopic ultrasound decreases bile duct injury: a multicenter study. Surg Endosc. 2009;23(2):384-8. Epub 2008 Jun 5.         [ Links ]

15. Davids PH, Tanka AK, Rauws EA, van Gulik TM, van Leeuwen DJ, de Witt LT, et al. Benign biliary strictures. Surgery or endoscopy? Ann Surg. 1993;217(3):237-43.         [ Links ]

16. Sikora SS, Srikanth G, Sarkari A, Kumar A. Hilar benign biliary strictures: need for subclassification. Aust N Z J Surg. 2003;73(7):484-8.         [ Links ]

17. Blumgart LH, Kelley CJ, Benjamin IS. Benign bile duct stricture following cholecystectomy: critical factors in management. Br J Surg. 1984;71(11):836-43.         [ Links ]

18. Mercado MA. Early versus late repair of bile duct injuries. Surg Endosc. 2006;20(11):1644-7. Epub 2006 Oct 23.         [ Links ]

19. Nealon WH, Urrutia F. Long-term follow-up after bilioenteric anastomosis for benign bile duct stricture. Ann Surg. 1996;223(6):639-45; discussion 645-8.         [ Links ]

20. de Santibañes E, Palavecino M, Ardiles V, Pekolj J. Bile duct injuries: management of late complications. Surg Endosc. 2006;20(11):1648-53. Epub 2006 Oct 23.         [ Links ]

21. Topal B, Aerts R, Penninckx F. The outcome of major biliary tract injury with leakage in laparoscopic cholecystectomy. Surg Endosc. 1999;13(1):53-6.         [ Links ]

22. Tsalis KG, Christoforidis EC, Dimitriadis CA, Kalfadis SC, Botsios DS, Dadoukis JD. Management of bile duct injury during and after laparoscopic cholecystectomy. Surg Endosc. 2003;17(1):31-7. Epub 2002 Oct 21.         [ Links ]

23. MacFadyen BV Jr, Vecchio R, Ricardo AE, Mathis CR. Bile duct injury after laparoscopic cholecystectomy. The United States experience. Surg Endosc. 1998;12(4):315-21.         [ Links ]

24. Huang CS, Lein HH, Tai FC, Wu CH. Long-term results of major bile duct injury associated with laparoscopic cholecystectomy. Surg Endosc. 2003;17(9):1362-7. Epub 2003 Jun 17.         [ Links ]

25. Lillemoe KD, Melton GB, Cameron JL, Pitt HA, Campbell KA, Talamini MA, et al. Postoperative bile duct strictures: management and outcome in the 1990s. Ann Surg. 2000;232(3):430-41.         [ Links ]

26. Bismuth H. The biliary tract. 9ª ed. Edinburgo: Churchill Living-stone; 1983.         [ Links ]

27. Alves A, Farges O, Nicolet J, Watrin T, Sauvanet A, Belghiti J. Incidence and consequence of an hepatic artery injury in patients with postcholecystectomy bile duct strictures. Ann Surg. 2003;238(1):93-6.         [ Links ]



Address for correspondence:
Fernando Barros
Work done at Hospital Geral de Bonsucesso
Rio de Janeiro - RJ, Brazil.

Received 07/10/2009
Accepted for publication 05/12/2009
Conflict of interest: none
Source of funding: none



How to cite this article: Barros F, Fernandes RA, Oliveira ME, Pacheco LF, Martinho JMS. The influence of time referral in the treatment of iatrogenic lesions of biliary tract . Rev Col Bras Cir. [periódico na Internet] 2010; 37(6). Disponível em URL:
Article from the thesis defended by Fernando de Barros in the Post-Graduate Program in Medical Sciences at the Universidade Federal Fluminense, as one of the requirements for obtaining the Master's Degree.

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License