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Iatrogenic injuries of the extrahepatic biliary system
j o u r n a l o f s u r g i c a l r e s e a r c h 1 j u n e 2 0 1 7 ( 2 1 3 ) 2 1 5 e2 2 1
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Iatrogenic injuries of the extrahepatic biliary system Ghodratollah Maddah, MD,a Mohammad Taghi Rajabi Mashhadi, MD,a Mehdi Parvizi Mashhadi, MD,a Mehdi Jabbari Nooghabi, PhD,b,c Masoumeh Hassanpour, MSc,b and Abbas Abdollahi, MDb,* a
Endoscopic and Minimally Invasive Surgery Research Center, Mashhad University of Medical Sciences, Mashhad, Iran b Surgical Oncology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran c Department of Statistics, Faculty of Mathematical Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
article info
abstract
Article history:
Background: Iatrogenic traumatic extrahepatic biliary tract injuries though rarely occur;
Received 28 May 2015
they can lead to exceedingly morbid complications. The aim of this study was to evaluate
Received in revised form
the management strategies and outcomes of patients presented with iatrogenic bile duct
10 October 2015
injuries.
Accepted 20 November 2015
Methods: This is a retrospective study. Over 19 y, 124 patients were managed for iatrogenic
Available online 25 November 2015
biliary injuries at our institution. The data related to the etiology of biliary tract injury, symptoms of injury, laboratory and radiologic studies, injury-to-diagnosis time, type of
Keywords:
biliary tract injury, injury management, hospitalization time, and postoperative compli-
Cholecystectomy
cations were reviewed.
Iatrogenic disease
Results: The main clinical presentations were jaundice or recurrent cholangitis in 64
Bile ducts
(51.61%) patients, followed by bile peritonitis in 34 (56.67%) and biliary fistula in 26 (43.33%)
Biliary stricture
patients. Only in 23 (18.54%) cases, the injury was recognized intraoperatively. The most frequent surgical procedure was open cholecystectomy in 81 (65.32%) of 124 patients. The remaining patients were operated on laparoscopically. Good results were achieved in 99 of 101 patients with direct suture repair including hepaticojejunostomy, choledocoduodenostomy, and choledochocholedochostomy (98.02% success rate) at the first attempt. Three cases (2.97%) of biliary strictures after direct suture technique and four (3.96%) cases of postoperative mortalities were detected. The mortality rate was mostly affected by male gender, advanced age, and existence of bile peritonitis. Totally, 111 (89.52%) patients are still alive with a mean follow-up time of 78 38 (2e230) mo. Conclusions: Biliary injuries can be sometimes life-threatening complications. A successful repair may provide patients with a lifelong relief from symptoms, whereas a failed repair may result in recurrent biliary obstruction, reoperation, and even death. ª 2015 Elsevier Inc. All rights reserved.
* Corresponding author. Surgical Oncology Research Center, Imam Reza Hospital, Faculty of Medicine, Mashhad University of Medical Sciences, 9133913716, Mashhad, Iran. Tel.: þ98 51 38022677; fax: þ98 51 38519868. E-mail address: [email protected] (A. Abdollahi). 0022-4804/$ e see front matter ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jss.2015.11.032
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Introduction Major bile duct injury is a life-threatening complication with severe financial implications.1 Cholecystectomy is a major surgical procedure which should never be assumed lightly.2,3 Even an experienced surgeon may cause accidental trauma to the biliary tract.4 Bile duct injury is associated with unfavorable long-term effects on health-related quality of life. The outcome of a litigation claim for malpractice can also affect quality of life.5 Cholecystectomy is one of the most frequently performed abdominal operations.6,7 Failure to identify the anatomy of the triangle of Calot has been revealed to be the commonest cause of biliary tract injury. This can be ascribed to the factors inherent to the laparoscopic approach, inadequate expertise of the surgeon, and local anatomic risk factors.8 The harmful effect of bile duct injury on survival can be avoided if surgeons, gastroenterologists, and radiologists work together in a multidisciplinary team.9 Open cholecystectomy is a reliable and secure method of gallbladder removal when performed by a trained surgeon.10 The incidence of bile duct injury during open cholecystectomy varies from 0%e0.4% and is most often reported at 0.1%e0.25%.11 But the rate of injury to the bile duct has increased and has at least doubled because the introduction of laparoscopic cholecystectomy.7 Despite an increasing number of surgeons with more experience in laparoscopic cholecystectomy, the incidence of iatrogenic injury to the bile duct continues to be stable; so it can be taken for granted that bile duct strictures and injuries will remain a problem well into the new millennium.12 Results of a survey in Vancouver general hospital showed that 57 (50%) of participating general surgeons experienced an injury to the bile duct during their practice.13 In recent years, we noticed a dramatic increase in the incidence of bile duct stricture and injuries due to introduction of a new generation of practicing surgeons and partly from the introduction of laparoscopic cholecystectomy. We present our experience with a series of patients who had iatrogenic biliary tract injury after cholecystectomy to evaluate the management strategies and outcomes of the patients.
The diagnosis of biliary injury was documented by clinical examination combined with the liver function tests studies. All injuries were detected by primary surgeons, and then, the patients were referred to our institution. Patients’ data were collected from the operative reports. The patients were recommended to return for follow-up visits and liver chemistry tests at 1, 3, 6, and 12 mo after discharge, then annually or as needed.
Technical considerations for reconstruction of hepaticojejunostomy In high bile duct injury, the procedure of lowering the hilar plate is performed. In this maneuver, an incision is made at the base of the quadrate lobe at the precise point in which Glisson capsule reflects to the lesser omentum. By elevation of the left hepatic system from under the surface of the caudate lobe, the exposure of the hilar bile duct will be facilitated. Bilioenteric anastomosis using the Roux-en-Y jejunal limb is a well-established approach. A Roux-en-Y loop of jejunum (70 cm in length) has to be prepared and brought up in a retrocolic fashion. A precise tension-free of unscarred mucosa is required. Special attention should be paid to the blood supply (back bleeding from the transected end of the upper bile duct) before creation of an anastomosis to prevent subsequent stricture formation and also for a better apposition of mucosa to mucosa anastomosis. We joined the mucosa to the jejunal serosa by 4-0 chromic stitch sutures as a separate stitches as shown in Figure 1. A single layer end to side anastomosis was made between the divided end of the duct and the jejunum. The anterior row of sutures was initially placed to raise the duct leaving a clear field for placement of the posterior row of sutures with the bites of 1e2 mm. We used 4-0, 5-0, or polyglactin braided suture (Supabon, Supa Medical Devices, Tehran, Iran) as a material for reconstruction of the bile duct.
Materials and methods This retrospective study was approved by the ethics committee of Mashhad University of Medical Sciences. Over 19 y from December 1994 to January 2014, 124 patients (30 [24.19%] male and 94 [75.81%] female with the mean age of 47.18 þ 13.99 y [aged 22e80 y]) were managed for iatrogenic biliary injuries at two teaching hospitals of Ghaem and Omid, affiliated to Mashhad University of Medical Sciences. Patient with minor bile leakage from the gallbladder bed was excluded. Major bile duct injuries included lateral lesions, complete transection, and late strictures of the extrahepatic bile ducts. We used Strasberg classification to describe the location of the extrahepatic bile duct injury in our survey.
Fig. 1 e Suturing of mucosa to serosa of the jejunal stoma preparing for anastomosis. (Color version of figure is available online.)
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maddah et al iatrogenic injuries of the extrahepatic biliary system
The posterior row of the interrupted sutures was placed with the knots tied within the lumen of the anastomosis before performing the anterior row of sutures. In cases with small lumen of anastomosis (below 1 cm), we usually passed a stent using a 12 or 14 French gage nelaton catheter into the right or left bile duct with the guide of Bake’s dilator out of a bile duct branch and through the liver parenchyma. The stent is then allowed to drain freely and usually after 10 to 14 d, it is cupped off by a heparin lock device, then the irrigation with 20 mL normal saline solution was started twice daily. The stent was removed 6 wk after the operation. When the hepatic bifurcation was destroyed, or if there was a transection of aberrant right hepatic duct, we joined the two ducts by stitch sutures of an absorbable material to provide a new common hepatic duct or anastomosed each duct separately to the jejunum.
Results The original procedures related to iatrogenic biliary tract injuries were open cholecystectomy in 81 (65.32%) patients and laparoscopic cholecystectomy in 43 (34.68%) patients. All open surgeries were performed between 1994 and 2014, but most laparoscopic procedures were carried out since 2009e2014. There were 30 (24.19%) male and 94 (75.81%) female with the average age of 47.18 þ 13.99 y (aged 22e80 y). The reason for iatrogenic injury was often difficult to determine in any particular case. However, according to the report from the first surgeon, cholecystectomy was performed in routine cases, so no reason for injury was identified in 102 (82.26%) cases. In the remaining 22 (17.74%) cases, the reasons recognized for occurring injuries included, attempts to control intraoperative bleeding in five (22.73%) patients and dense adhesions in 17 (77.27%) cases. The difference was significant (P ¼ 0.011). The main clinical presentations were jaundice, or recurrent cholangitis in 64 (51.61%) patients (respectively in 37 [57.81%] and 27 [42.19%] patients, and the difference was not significant; P ¼ 0.211), bile peritonitis in 34 (56.67%) patients and biliary fistula in 26 (43.33%) patients, and there was no significant different (P ¼ 0.302). The mean serum total bilirubin level was 12.27 þ 11.96 mg/ dL (range, 0.7e44.6 mg/dL, normal range, 0.3e1 mg/dL), serum glutamic-oxaloacetic transaminase 87.26 þ 69.39 mL (range, 13e425, normal range, 5e40 mL), serum glutamic-pyruvic transaminase 102.38 þ 108.16 mL (range, 9e932, normal range, 5e50 mL), alkaline phosphatase 920.26 þ 908.07 mL (range 112e7972, normal range 35e135 mL). Based on Strasberg classification, the location of the extrahepatic bile duct injury in 124 patients is shown in Table 1. The difference was significant (P < 0.001). Only in 23 (18.54%) cases, the injury was recognized at the time of operation. In the remaining 101 patients, the mean time of injury recognition (the time from occurring bile duct injury to the first attempt for repairing the damage) was 44.40 þ 54.50 d (ranged 3e330 d). The types of injuries of common or hepatic bile duct injuries that we encountered were complete or partial transection of common hepatic duct in 119 (95.97%) patients, short cystic duct resulting in narrowing of common bile duct in one
Table 1 e Strasberg classification of bile duct injury in 124 cases. Type
No
Percent
Criteria
A
3
2.42
Cystic duct leak or leak from small ducts in the liver bed
B
0
0
Occlusion of an aberrant right hepatic duct
C
1
0.81
Transection without ligation of an aberrant right hepatic duct Lateral injury to a major bile duct
D
4
3.23
E1
18
14.52
Transection >2 cm from the hilum
E2
32
25.81
Transection <2 cm from the hilum
E3
54
43.55
Transection in the hilum
E4
9
7.26
Separation of major ducts in the hilum
E5
3
2.42
Type C injury plus injury in the hilum
(0.81%), cystic leakage due to retained distal choledochal stone in one (0.81%), clips or sutures around the choledochus in two (1.61%), and inadvertent anastomosis of Hartmann’s pouch presumed to be choledochus in one (0.81%) patient, and the difference was significant (P < 0.001). As a result of previous attempts by primary surgeons, 64 (51.61%) patients developed postcholecystectomy bile duct stricture or biliary fistula (Table 2). Also, 60 (48.39%) patients were referred without any further operations beforehand. All patients were referred from different institutions. So a total of 124 patients were presented for definitive surgery. The definitive surgery for biliary duct repair included hepaticojejunostomy in 99 (79.84%) patients, choledochoduodenostomy in two (1.61%) patients, T-tube insertion in nine (7.26%) patients, hilar drainage via laparotomy in nine (7.26%) patients. Other techniques in five (4.03%) patients (there was significant difference; P < 0.001) included completion of cholecystectomy and ligation of open cystic duct and removal of retained choledochal stone in one (20.00%) patient, primary repair of choledochus in one (20.00%) patient, removal of clips around the choledochus and insertion of T-tube in one (20.00%) patient, ligation of aberrant right hepatic duct in one (20.00%) patient and completion of cholecystectomy and discard of cholecystoduodenostomy and repair of duodenum in one (20.00%) patient. In the latter patient, the gallbladder was mistakenly considered to be the choledochus by the first surgeon, and cholecystoduodenostomy was performed. In performing 99 (79.84%) hepaticojejunostomy during definitive surgery, we used 29 (29.29%) transhepatic stents including 19 (65.52%) stents into the right hepatic ducts, eight (27.59%) into the left and two (6.89%) stents into both left and right hepatic ducts in the two remaining patients. In nine (37.50%) patients, the hepatic bifurcation was destroyed with two separate lumens of right and left hepatic duct and also in three patients, there (12.50%) was a transection of right aberrant hepatic duct simultaneously to injury of the main hepatic duct at the hilum (E5 Strasberg classification). To address in these complicated cases, we performed each duct anastomosis to jejunum separately in five (20.83%)
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Table 2 e The types of previous attempts for treatment of bile duct injuries in 64 patients. Type of injury
No (%)
Initial procedure Type
Trauma recognized simultaneous to cholecystectomy
23 (35.94)
External drainage or T-tube
41 (64.06)
6 (26.09)
Choledocoduodenostomy
6 (26.09) 0.337
Irrigation and drainage via laparotomy T-tube
Hepaticojejunostomy
0.024
35 for 24 (58.54) patients 1 (2.44)
Choledocoduodenostomy
P value
11 (47.83)
Hepaticojejunostomy
P value Trauma recognized late after cholecystectomy
No (%)
3 (7.32) 7 for 5 (12.20) patients
Endoscopic procedures*
6 (14.63)
Choledochocholedochostomy
1 (2.44)
Removal of suture around choleduchus
1 (2.44)
P value
<0.001
*
Endoscopic procedures include balloon dilation in three (60.00%) patients, papillary sphincterotomy resulting in duodenal perforation and death in one (20.00%) patient and plastic stent in one (20.00%) patient, and the difference was not significant (P ¼ 0.449).
cases, and approximation of medial side of ducts to each other to provide a new common duct for anastomosis in six (25.00%) cases and ligation of the aberrant right hepatic duct without any consequences in one (4.17%) case. There was no significant difference (P ¼ 0.105). A good result on the first attempt was achieved in 99 of 101 patients with direct suture repair (98.02%, success rate). Biliary stricture was developed in three (42.86%) patients, which was successfully managed by rehepaticojejunostomy in one patient. In the second patient, we could not find any duct at the hilum for rehepaticojejunostomy, so we performed segment three cholangiojejunostomy, which was unsuccessful, and the patient died postoperatively. The third patient who developed biliary stricture 12 mo after reconstruction was referred for radiologic balloon dilation, which unfortunately was unsuccessful and the patient died. The median time for development of stricture after hepaticojejunostomy was 10 (range, 6e12 mo) mo. Overall, the ultimate success rate for direct suture technique was 96.03% (97 of 101 cases). The outcome of direct suture technique is shown in Table 3. Totally, four (3.23%) mortalities occurred in direct suture repair: two (50.00%) early postoperative mortalities due to intraperitoneal sepsis and two (50.00%) late mortalities due to biliary stricture and recurrent cholangitis after
hepaticojejunostomy. Also, nine (7.26%) mortalities observed after nondirect repair. These patients were operated on for bile peritonitis using open drainage of the hilum (9 of 34 [26.47%] bile peritonitis were expired). Male gender and advanced age were associated with higher rate of mortality (Table 4). On the whole, 111 patients are still alive with overall success rate of 89.52% with a mean follow-up of 78 38 mo (2e230 mo), and 13 patients died (mortality rate of 10.48%).
Discussion In our study, the injuries were initiated by open cholecystectomy in 81 (65.32%) patients and laparoscopic cholecystectomy in 43 (34.68%) patients. Owing to novelty of laparoscopic surgeries in our institution, the overall rate of laparoscopy and the rate of laparoscopic-induced bile duct injuries were lower than that of open procedures. Most iatrogenic injuries to major bile duct during cholecystectomy are not recognized during the operation, rather may appear several days or weeks later as a bile peritonitis, biliary fistula, or progressive jaundice.14 Approximately one fourth of all major bile duct injuries are noted at the time of operation. More than three quarters of iatrogenic major bile duct injuries remain unrecognized during
Table 3 e The outcome of direct suture repair in 101 patients with a median follow-up time of 76 mo (range, 0.5e230 mo). Complication
No (%)
Procedure
Outcome
Bile stricture
3 (42.86)
Rehepaticojejunostomy in one patient Segment III cholangiojejunostomy in one patient Balloon dilatation of bile stricture under imaging guidance in one patient
Recovered Died Died
Generalized peritonitis (unknown origin)*
1 (14.29)
Irrigation and peritoneal drainage
Recovered
Hemorrhagic shock due to falciform ligament bleeding
1 (14.29)
Ligation of bleeding points with suture
Recovered
Postoperative intraperitoneal sepsis
2 (28.57)
Medical treatment
2 died
P value *
0.666
d
This patient had a liver abscess which was drained simultaneously with hepaticojejunostomy.
d
maddah et al iatrogenic injuries of the extrahepatic biliary system
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Table 4 e Distribution of mortality in each factor. Mortality
Expired
Survived
Total
P value
Type of operation Laparoscopy
4 (9.30%)
39 (90.70%)
43 (34.68%)
Open
9 (11.11%)
72 (88.89%)
81 (65.32%)
62.15 þ 12.92
45.38 þ 13.06
47.18 þ 13.99
Peritonitis
9 (26.47%)
25 (73.53%)
34 (27.42%)
Nonperitonitis
4 (4.44%)
86 (95.56%)
90 (72.58%)
Age (y)
0.996 <0.001
Presentation 0.001
Gender Male
6 (20.00%)
24 (80.00%)
30 (24.19%)
Female
7 (7.45%)
87 (92.55%)
94 (75.81%)
13.7 þ 4.83
20 þ 7.00
19.34 þ 5.92
<0.001
0.011
Time of injury recognition for bile peritonitis (d)
0.107
Gender in relation to bile peritonitis Male
5 (71.43%)
2 (28.57%)
7 (20.59%)
Female
4 (14.81%)
23 (85.19%)
27 (79.41%)
Age in relation to bile peritonitis (y) Male
63.6 5.5 (range, 47e80)
Female
60.6 þ 6.7 (range, 35e75)
the operations.15,16 However, in our series, only 19% (23 cases) of injuries were discovered at the time of cholecystectomy. The mean time for delayed recognition of injury in our series was 44.9 d. This is in contrast with other reported series with mean range of 12 and 16 d delay in recognition of injuries.10,17 Because of missing data, we cannot precisely justify the long delay in diagnosis of injury. However, it may be due to less severe injuries. The mean time of injury recognition for bile peritonitis in the dead patients was 13.7 d in contrast to 19.5 d in survivors. This is in conflict with the common sense that with earlier diagnosis the better prognosis is expected in the bile peritonitis patients. We assume that this increased mortality is probably due to bacterial peritonitis or physiologic state of the dead patients that worsened the condition of patient which mandates the physician to recognize the diagnosis of bile peritonitis earlier. Jaundice and cholangitis were the most common presenting manifestations in the present study (51.6%), followed by bile peritonitis (27.4%) and external fistula (20.9%). In a study by Pitt et al. 16 on 106 patients with postoperative bile duct injury, 77% of patients became jaundiced, and an external biliary fistula or bile peritonitis occurred in 14% and 43% of their patients, respectively. The localization of a bile duct stricture is of highest importance not only for proper management but also to determine the prognosis. There is a variety of classification systems developed to elucidate bile duct injuries with regard to anatomy. Bismuth developed a classification of bile duct strictures based on the anatomic patterns of involvement.6 Strasberg modified the original Bismuth classification into a more comprehensive system, which we chose for defining the anatomy of bile duct injuries. In Glenn’s report of 100 biliary tract injuries after open cholecystectomy, the most common site of injury was the cystic duct-common hepatic junction (58%).18 The most common site of injury in our study was transection in the
hilum (in the rate of 42.7%), which was in accordance with type E3 injuries in the Strasberg classification. The purpose of surgical repair in biliary tract injuries is to restore a durable bile conduit and to prevent both short-term and long-term complications, such as stricture and cholangitis.1 If the injury to the bile duct is recognized during cholecystectomy, it is then quite tempting to attempt a complex repair. The surgeon should assess the situation in terms of his own ability to deal with the problem. The surgeon should not underestimate the emotional impact of these injuries on his or her ability to perform definitive reconstruction. The surgeon should not also hesitate to ask for assistance from a more experienced surgeon, or it may be apt to provide external biliary drainage by means of proximal intubations and then refer the patient for definitive management to a center having expertise in such complex problems.14,19 The most favorable management is dependent on the timing of recognition of injury, the extent of bile duct injury, the patient’s condition, and the availability of experienced hepatobiliary surgeons.20 Bile peritonitis is the most crucial and potentially fatal consequence of the bile leakage.21 When septic bile peritonitis is present, laparotomy is indicated without further investigations.22 In this situation, because of bile ducts collapse and extreme staining of the tissues with bile, a definitive repair is scarcely possible. The goal then should be open drainage. The definitive reconstruction may be delayed until a subsequent date. In some patients, we performed multiple irrigation and drainage procedures. Mathews and Blumgart 14 suggested that the open drainage may be carried out through a mobilized Roux-en-y loop of jejunum with the open drainage tube simply being led in a transjejunal fashion to the exterior. Such a procedure permits initial control, and most often inevitably requires reoperation for bile duct stenosis.3
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In this situation, we preferred open drainage and late biliary reconstruction as needed. In construction of hepaticojejunostomy, few points should be considered. The criteria necessary for a successful biliary tract reconstruction have been listed by Rodney Smith as making the largest possible stoma, accurate apposition of mucosa to mucosa at all points around the stoma and an adequate blood supply.23 Mucosa to mucosa apposition is a basic requirement for obtaining long-term anastomotic patency, and all efforts should be made to reach this goal.24 For better apposition of mucosa to mucosa anastomosis, Breach et al. 25 advocated using a loop on the mucosa stitch to apply jejunal mucosa directly to the ductal mucosa. Considerable questions regarding the use of internal stenting and the optimal time for stenting of reconstructive procedure, whether decreases the stricture formation still remain unanswered. Some authors are skeptical about the value of stent, and rarely use transanastomotic splinting, however, they obtained good results.18,20,26 Bismuth et al. reported 123 patients with benign diseases who underwent Roux-en-y hepaticojejunostomy. In no instance was a stent used; only one instance of anastomotic stenosis was observed during a follow-up study averaging 5.5 y.26 On the other hand, several investigators feel strongly that stents are beneficial and claim that avoiding using stents may lead to recurrent cholangitis.17 They noted that it provides an adequate biliary drainage in the postoperative period and allows irrigation with sterile water to keep the bile passage clear of debris and cholangiograms are easily performed through the tube.23 Prolonged patency could also be expected in case of formation of collagen scar.27 Some experienced surgeons have advocated leaving splints in place for months to 2 y or until they become occluded.25 However, some authors believe that the best results appeared to be achieved in those patients who are intubated for 1 to 3 mo. The beneficial use of a tube deteriorates with prolonged use (longer than 3 mo) because of inflammation caused by a foreign body.27 In constructing hepaticojejunostomy when the lumen of anastomosis seems to be <1 cm, we usually use a transanastomotic stent which passes retrograde from the ducts out through the surface of the liver inside the Roux limb. The transhepatic tube was connected to external drainage until day 10 after surgery when cholangiography was performed. If no leakage was detected, the tube was closed and left in place then was removed after 6 wk. Although the short-term consequences of major bile duct injury and stricture are significant, it is the long-term outcome after repair that serves as the primary determinant of resolution of the complications. Lillemoe et al. 12 described the outcome of 156 patients after surgical reconstruction for bile duct strictures with a mean follow-up of 57.5 mo which showed overall success rate of 90.8% and one case of mortality due to pulmonary embolism. Pitt et al. 16 reported that by 3 y after a repair, only two-thirds of the patients who eventually had a recurrent stricture returned for reoperation, and even 5 y after operation for benign postoperative stricture, only 80% of recurrences occurred. Another
analysis underscores the need for prolonged follow-up in determining the results of surgery in these patients, so close surveillance for at least 5 y is mandatory after a stricture repair.19 In this study, the average follow-up period was 78 mo with a success rate of 98% with direct suture techniques at first attempt of reconstruction and ultimately a good result in 96% patients during this period. In this study, we found three biliary strictures of 101 cases of direct suture technique. The mean time for development of stricture was 10 mo after biliary reconstruction. The overall mortality rate in our study of patients was 11.5% (13 patients). This mortality rate is similar to other reports that have noted an early mortality rate ranging from 11%e18% in severely ill patients.10 Factors affecting mortality in our series were advanced age, male gender, and presentation with bile peritonitis (Table 4). Considering the introduction of laparoscopy in the last decade in Iran, in our study, there has been a high proportion of open surgery versus laparoscopic procedure, so we cannot compare biliary tract injuries in terms of the two surgical approaches. It can be acknowledged as a limitation of our study.
Conclusion The incidence of iatrogenic bile duct injuries has recently increased and has been associated with increased use of laparoscopic cholecystectomy worldwide. It is essential to be careful in the proper visualization of the surgical area and the identification of structures before ligation or transection to decrease the risk of bile duct injuries during surgery. When biliary injury develops, early recognition and appropriate treatment are of highest importance. Early and appropriate treatment allows avoidance of serious complications in patients with iatrogenic bile duct injuries. After bile duct repair, patients require long-term and careful postoperative observation because of the possibility of biliary anastomosis stricture.
Acknowledgment The results described in this article formed part of a thesis submitted by the third author to the Mashhad University of Medical Sciences for a postgraduate degree in general surgery. The study was supported by the Vice Chancellor for Research of Mashhad University of Medical Sciences (grant number: 920457). There was no funding obtained for the article. Authors contributions: Abdollahi Abbas, Maddah Ghodratollah, Rajabi Mashhadi Mohammad Taghi performed the conception and design. Abdollahi Abbas, Maddah Ghodratollah, Rajabi Mashhadi Mohammad Taghi contributed to analysis and/or interpretation of data. Maddah Ghodratollah, Rajabi Mashhadi Mohammad Taghi, Abdollahi Abbas, Parvizi Mashhadi Mehdi performed the data. Maddah Ghodratollah, Abdollahi Abbas, Parvizi Mashhadi Mehdi, Hassanpour Masoumeh wrote the article. Maddah Ghodratollah, Rajabi Mashhadi Mohammad Taghi, Abdollahi Abbas, Parvizi Mashhadi Mehdi, Jabbari Nooghabi Mehdi, Hassanpour Masoumeh
maddah et al iatrogenic injuries of the extrahepatic biliary system
performed the critical revision of data. Maddah Ghodratollah, Abdollahi Abbas, Jabbari Nooghabi Mehdi, Hassanpour Masoumeh performed the final approval. Jabbari Nooghabi Mehdi performed the statistical analysis. Maddah Ghodratollah, Abdollahi Abbas took the overall responsiblity.
Disclosure The authors declare no conflicts of interest.
references
1. Schmidt SC, Langrehr JM, Hintze RE, Neuhaus P. Long-term results and risk factors influencing outcome of major bile duct injuries following cholecystectomy. Br J Surg. 2005;92:76. 2. Andre´n-Sandberg A, Alinder G, Bengmark S. Accidental lesions of the common bile duct at cholecystectomy. Pre- and perioperative factors of importance. Ann Surg. 1985;201:328. 3. Retirada de Mattheus JB, Blumgart LH. Benign biliary strictures. In: Zinner MJ, Schwartz SI, Ellis H, eds. Maingot’s abdominal operations. Connecticut: Appleton and Lange; 1997:1803. 4. Garden OJ. Iatrogenic injury to the bile duct. Br J Surg. 1991;78:1412. 5. de Reuver PR, Sprangers MA, Rauws EA, et al. Impact of bile duct injury after laparoscopic cholecystectomy on quality of life: a longitudinal study after multidisciplinary treatment. Endoscopy. 2008;40:637. 6. Yeo CJ, Lillemoe KD, Ahrendt SA, Pitt HA. Operative management of strictures and benign obstructive disorders of the bile duct. In: Zuidema GD, Yeo CJ, Orringer MB, eds. Shackelford’s surgery of the alimentary tract. Philadelphia: WB Saunders Company; 2002:247. 7. Parmeggiani D, Cimmino G, Cerbone D, et al. Biliary tract injuries during laparoscopic cholecystectomy: three case reports and literature review. G Chir. 2010;31:16. 8. Ahrendt SA, Pitt HA. Surgical therapy of iatrogenic lesions of biliary tract. World J Surg. 2001;25:1360. 9. de Reuver PR, Rauws EA, Bruno MJ, et al. Survival in bile duct injury patients after laparoscopic cholecystectomy: a multidisciplinary approach of gastroenterologists, radiologists, and surgeons. Surgery. 2007;142:1. 10. Kern KA. Medicolegal analysis of bile duct injury during open cholecystectomy and abdominal surgery. Am J Surg. 1994;168:217.
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11. 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;165:9. 12. Lillemoe KD, Melton GB, Cameron JL, et al. Postoperative bile duct strictures: management and outcome in the 1990s. Ann Surg. 2000;232:430. 13. Francoeur JR, Wiseman K, Buczkowski AK, Chung SW, Scudamore CH. Surgeons’ anonymous response after bile duct injury during cholecystectomy. Am J Surg. 2003;185:468. 14. Roslyn JJ, Tompkins RK. Reoperation for biliary strictures. Surg Clin North Am. 1991;71:109. 15. Millis JM, Tompkins RK, Zinner MJ, Longmire Jr WP, Roslyn JJ. Management of bile duct strictures. An evolving strategy. Arch Surg. 1992;127:1077. discussion 1082e4. 16. Pitt HA, Miyamoto T, Parapatis SK, Tompkins RK, Longmire Jr WP. Factors influencing outcome in patients with postoperative biliary strictures. Am J Surg. 1982;144:14. 17. Browder IW, Dowling JB, Koontz KK, Litwin MS. Early management of operative injuries of the extrahepatic biliary tract. Ann Surg. 1987;205:649. 18. Gelenn F. Iatrogenic injuries to the biliary duct of system. Surg Gynecol Obstet. 1978;146:430. 19. Pitt HA. Benign biliary stricture. In: Carter DC, Russell RCG, Pitt HA, Bismuth H, eds. Rob & Smith’s Operative Surgery Hepatobiliary and Pancreatic Surgery. London: Chapman & Hall; 1996:370. 20. Lau WY, Lai EC, Lau SH. Management of bile duct injury after laparoscopic cholecystectomy: a review. ANZ J Surg. 2010;80:75. 21. Morgenstern L. Early diagnosis of bile leakage. In: Berci G, Cuschieri A, eds. Bile ducts and bile duct stones. Philadelphia: W. B. Saunders Company; 1997:130. 22. Deziel DJ. Complications of cholecystectomy. Incidence, clinical manifestations, and diagnosis. Surg Clin North Am. 1994;74:809. 23. Moossa AR, Block GE, Skinner DB, Hall AW. Reconstruction of high biliary tract strictures employing transhepatic intubation. Surg Clin North Am. 1976;56:73. 24. Machado MC, da Cunha JE, Bacchella T. A modified technique for surgical repair of cicatricial stenosis of the bile duct. Surg Gynecol Obstet. 1986;162:282. 25. Braasch JW, Bolton JS, Rossi RL. A technique of biliary tract reconstruction with complete follow up in 44 consecutive cases. Ann Surg. 1981;194:635. 26. Bismuth H, Franco D, Corlette MB, Hepp J. Long term results of Roux-en-Y hepaticojejunostomy. Surg Gynecol Obstet. 1978;146:161. 27. Way LW, Dunphy JE. Biliary stricture. Am J Surg. 1972;124:287.
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Iatrogenic injuries of the extrahepatic biliary system Ghodratollah Maddah, MD,a Mohammad Taghi Rajabi Mashhadi, MD,a Mehdi Parvizi Mashhadi, MD,a Mehdi Jabbari Nooghabi, PhD,b,c Masoumeh Hassanpour, MSc,b and Abbas Abdollahi, MDb,* a
Endoscopic and Minimally Invasive Surgery Research Center, Mashhad University of Medical Sciences, Mashhad, Iran b Surgical Oncology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran c Department of Statistics, Faculty of Mathematical Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
article info
abstract
Article history:
Background: Iatrogenic traumatic extrahepatic biliary tract injuries though rarely occur;
Received 28 May 2015
they can lead to exceedingly morbid complications. The aim of this study was to evaluate
Received in revised form
the management strategies and outcomes of patients presented with iatrogenic bile duct
10 October 2015
injuries.
Accepted 20 November 2015
Methods: This is a retrospective study. Over 19 y, 124 patients were managed for iatrogenic
Available online 25 November 2015
biliary injuries at our institution. The data related to the etiology of biliary tract injury, symptoms of injury, laboratory and radiologic studies, injury-to-diagnosis time, type of
Keywords:
biliary tract injury, injury management, hospitalization time, and postoperative compli-
Cholecystectomy
cations were reviewed.
Iatrogenic disease
Results: The main clinical presentations were jaundice or recurrent cholangitis in 64
Bile ducts
(51.61%) patients, followed by bile peritonitis in 34 (56.67%) and biliary fistula in 26 (43.33%)
Biliary stricture
patients. Only in 23 (18.54%) cases, the injury was recognized intraoperatively. The most frequent surgical procedure was open cholecystectomy in 81 (65.32%) of 124 patients. The remaining patients were operated on laparoscopically. Good results were achieved in 99 of 101 patients with direct suture repair including hepaticojejunostomy, choledocoduodenostomy, and choledochocholedochostomy (98.02% success rate) at the first attempt. Three cases (2.97%) of biliary strictures after direct suture technique and four (3.96%) cases of postoperative mortalities were detected. The mortality rate was mostly affected by male gender, advanced age, and existence of bile peritonitis. Totally, 111 (89.52%) patients are still alive with a mean follow-up time of 78 38 (2e230) mo. Conclusions: Biliary injuries can be sometimes life-threatening complications. A successful repair may provide patients with a lifelong relief from symptoms, whereas a failed repair may result in recurrent biliary obstruction, reoperation, and even death. ª 2015 Elsevier Inc. All rights reserved.
* Corresponding author. Surgical Oncology Research Center, Imam Reza Hospital, Faculty of Medicine, Mashhad University of Medical Sciences, 9133913716, Mashhad, Iran. Tel.: þ98 51 38022677; fax: þ98 51 38519868. E-mail address: [email protected] (A. Abdollahi). 0022-4804/$ e see front matter ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jss.2015.11.032
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Introduction Major bile duct injury is a life-threatening complication with severe financial implications.1 Cholecystectomy is a major surgical procedure which should never be assumed lightly.2,3 Even an experienced surgeon may cause accidental trauma to the biliary tract.4 Bile duct injury is associated with unfavorable long-term effects on health-related quality of life. The outcome of a litigation claim for malpractice can also affect quality of life.5 Cholecystectomy is one of the most frequently performed abdominal operations.6,7 Failure to identify the anatomy of the triangle of Calot has been revealed to be the commonest cause of biliary tract injury. This can be ascribed to the factors inherent to the laparoscopic approach, inadequate expertise of the surgeon, and local anatomic risk factors.8 The harmful effect of bile duct injury on survival can be avoided if surgeons, gastroenterologists, and radiologists work together in a multidisciplinary team.9 Open cholecystectomy is a reliable and secure method of gallbladder removal when performed by a trained surgeon.10 The incidence of bile duct injury during open cholecystectomy varies from 0%e0.4% and is most often reported at 0.1%e0.25%.11 But the rate of injury to the bile duct has increased and has at least doubled because the introduction of laparoscopic cholecystectomy.7 Despite an increasing number of surgeons with more experience in laparoscopic cholecystectomy, the incidence of iatrogenic injury to the bile duct continues to be stable; so it can be taken for granted that bile duct strictures and injuries will remain a problem well into the new millennium.12 Results of a survey in Vancouver general hospital showed that 57 (50%) of participating general surgeons experienced an injury to the bile duct during their practice.13 In recent years, we noticed a dramatic increase in the incidence of bile duct stricture and injuries due to introduction of a new generation of practicing surgeons and partly from the introduction of laparoscopic cholecystectomy. We present our experience with a series of patients who had iatrogenic biliary tract injury after cholecystectomy to evaluate the management strategies and outcomes of the patients.
The diagnosis of biliary injury was documented by clinical examination combined with the liver function tests studies. All injuries were detected by primary surgeons, and then, the patients were referred to our institution. Patients’ data were collected from the operative reports. The patients were recommended to return for follow-up visits and liver chemistry tests at 1, 3, 6, and 12 mo after discharge, then annually or as needed.
Technical considerations for reconstruction of hepaticojejunostomy In high bile duct injury, the procedure of lowering the hilar plate is performed. In this maneuver, an incision is made at the base of the quadrate lobe at the precise point in which Glisson capsule reflects to the lesser omentum. By elevation of the left hepatic system from under the surface of the caudate lobe, the exposure of the hilar bile duct will be facilitated. Bilioenteric anastomosis using the Roux-en-Y jejunal limb is a well-established approach. A Roux-en-Y loop of jejunum (70 cm in length) has to be prepared and brought up in a retrocolic fashion. A precise tension-free of unscarred mucosa is required. Special attention should be paid to the blood supply (back bleeding from the transected end of the upper bile duct) before creation of an anastomosis to prevent subsequent stricture formation and also for a better apposition of mucosa to mucosa anastomosis. We joined the mucosa to the jejunal serosa by 4-0 chromic stitch sutures as a separate stitches as shown in Figure 1. A single layer end to side anastomosis was made between the divided end of the duct and the jejunum. The anterior row of sutures was initially placed to raise the duct leaving a clear field for placement of the posterior row of sutures with the bites of 1e2 mm. We used 4-0, 5-0, or polyglactin braided suture (Supabon, Supa Medical Devices, Tehran, Iran) as a material for reconstruction of the bile duct.
Materials and methods This retrospective study was approved by the ethics committee of Mashhad University of Medical Sciences. Over 19 y from December 1994 to January 2014, 124 patients (30 [24.19%] male and 94 [75.81%] female with the mean age of 47.18 þ 13.99 y [aged 22e80 y]) were managed for iatrogenic biliary injuries at two teaching hospitals of Ghaem and Omid, affiliated to Mashhad University of Medical Sciences. Patient with minor bile leakage from the gallbladder bed was excluded. Major bile duct injuries included lateral lesions, complete transection, and late strictures of the extrahepatic bile ducts. We used Strasberg classification to describe the location of the extrahepatic bile duct injury in our survey.
Fig. 1 e Suturing of mucosa to serosa of the jejunal stoma preparing for anastomosis. (Color version of figure is available online.)
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maddah et al iatrogenic injuries of the extrahepatic biliary system
The posterior row of the interrupted sutures was placed with the knots tied within the lumen of the anastomosis before performing the anterior row of sutures. In cases with small lumen of anastomosis (below 1 cm), we usually passed a stent using a 12 or 14 French gage nelaton catheter into the right or left bile duct with the guide of Bake’s dilator out of a bile duct branch and through the liver parenchyma. The stent is then allowed to drain freely and usually after 10 to 14 d, it is cupped off by a heparin lock device, then the irrigation with 20 mL normal saline solution was started twice daily. The stent was removed 6 wk after the operation. When the hepatic bifurcation was destroyed, or if there was a transection of aberrant right hepatic duct, we joined the two ducts by stitch sutures of an absorbable material to provide a new common hepatic duct or anastomosed each duct separately to the jejunum.
Results The original procedures related to iatrogenic biliary tract injuries were open cholecystectomy in 81 (65.32%) patients and laparoscopic cholecystectomy in 43 (34.68%) patients. All open surgeries were performed between 1994 and 2014, but most laparoscopic procedures were carried out since 2009e2014. There were 30 (24.19%) male and 94 (75.81%) female with the average age of 47.18 þ 13.99 y (aged 22e80 y). The reason for iatrogenic injury was often difficult to determine in any particular case. However, according to the report from the first surgeon, cholecystectomy was performed in routine cases, so no reason for injury was identified in 102 (82.26%) cases. In the remaining 22 (17.74%) cases, the reasons recognized for occurring injuries included, attempts to control intraoperative bleeding in five (22.73%) patients and dense adhesions in 17 (77.27%) cases. The difference was significant (P ¼ 0.011). The main clinical presentations were jaundice, or recurrent cholangitis in 64 (51.61%) patients (respectively in 37 [57.81%] and 27 [42.19%] patients, and the difference was not significant; P ¼ 0.211), bile peritonitis in 34 (56.67%) patients and biliary fistula in 26 (43.33%) patients, and there was no significant different (P ¼ 0.302). The mean serum total bilirubin level was 12.27 þ 11.96 mg/ dL (range, 0.7e44.6 mg/dL, normal range, 0.3e1 mg/dL), serum glutamic-oxaloacetic transaminase 87.26 þ 69.39 mL (range, 13e425, normal range, 5e40 mL), serum glutamic-pyruvic transaminase 102.38 þ 108.16 mL (range, 9e932, normal range, 5e50 mL), alkaline phosphatase 920.26 þ 908.07 mL (range 112e7972, normal range 35e135 mL). Based on Strasberg classification, the location of the extrahepatic bile duct injury in 124 patients is shown in Table 1. The difference was significant (P < 0.001). Only in 23 (18.54%) cases, the injury was recognized at the time of operation. In the remaining 101 patients, the mean time of injury recognition (the time from occurring bile duct injury to the first attempt for repairing the damage) was 44.40 þ 54.50 d (ranged 3e330 d). The types of injuries of common or hepatic bile duct injuries that we encountered were complete or partial transection of common hepatic duct in 119 (95.97%) patients, short cystic duct resulting in narrowing of common bile duct in one
Table 1 e Strasberg classification of bile duct injury in 124 cases. Type
No
Percent
Criteria
A
3
2.42
Cystic duct leak or leak from small ducts in the liver bed
B
0
0
Occlusion of an aberrant right hepatic duct
C
1
0.81
Transection without ligation of an aberrant right hepatic duct Lateral injury to a major bile duct
D
4
3.23
E1
18
14.52
Transection >2 cm from the hilum
E2
32
25.81
Transection <2 cm from the hilum
E3
54
43.55
Transection in the hilum
E4
9
7.26
Separation of major ducts in the hilum
E5
3
2.42
Type C injury plus injury in the hilum
(0.81%), cystic leakage due to retained distal choledochal stone in one (0.81%), clips or sutures around the choledochus in two (1.61%), and inadvertent anastomosis of Hartmann’s pouch presumed to be choledochus in one (0.81%) patient, and the difference was significant (P < 0.001). As a result of previous attempts by primary surgeons, 64 (51.61%) patients developed postcholecystectomy bile duct stricture or biliary fistula (Table 2). Also, 60 (48.39%) patients were referred without any further operations beforehand. All patients were referred from different institutions. So a total of 124 patients were presented for definitive surgery. The definitive surgery for biliary duct repair included hepaticojejunostomy in 99 (79.84%) patients, choledochoduodenostomy in two (1.61%) patients, T-tube insertion in nine (7.26%) patients, hilar drainage via laparotomy in nine (7.26%) patients. Other techniques in five (4.03%) patients (there was significant difference; P < 0.001) included completion of cholecystectomy and ligation of open cystic duct and removal of retained choledochal stone in one (20.00%) patient, primary repair of choledochus in one (20.00%) patient, removal of clips around the choledochus and insertion of T-tube in one (20.00%) patient, ligation of aberrant right hepatic duct in one (20.00%) patient and completion of cholecystectomy and discard of cholecystoduodenostomy and repair of duodenum in one (20.00%) patient. In the latter patient, the gallbladder was mistakenly considered to be the choledochus by the first surgeon, and cholecystoduodenostomy was performed. In performing 99 (79.84%) hepaticojejunostomy during definitive surgery, we used 29 (29.29%) transhepatic stents including 19 (65.52%) stents into the right hepatic ducts, eight (27.59%) into the left and two (6.89%) stents into both left and right hepatic ducts in the two remaining patients. In nine (37.50%) patients, the hepatic bifurcation was destroyed with two separate lumens of right and left hepatic duct and also in three patients, there (12.50%) was a transection of right aberrant hepatic duct simultaneously to injury of the main hepatic duct at the hilum (E5 Strasberg classification). To address in these complicated cases, we performed each duct anastomosis to jejunum separately in five (20.83%)
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Table 2 e The types of previous attempts for treatment of bile duct injuries in 64 patients. Type of injury
No (%)
Initial procedure Type
Trauma recognized simultaneous to cholecystectomy
23 (35.94)
External drainage or T-tube
41 (64.06)
6 (26.09)
Choledocoduodenostomy
6 (26.09) 0.337
Irrigation and drainage via laparotomy T-tube
Hepaticojejunostomy
0.024
35 for 24 (58.54) patients 1 (2.44)
Choledocoduodenostomy
P value
11 (47.83)
Hepaticojejunostomy
P value Trauma recognized late after cholecystectomy
No (%)
3 (7.32) 7 for 5 (12.20) patients
Endoscopic procedures*
6 (14.63)
Choledochocholedochostomy
1 (2.44)
Removal of suture around choleduchus
1 (2.44)
P value
<0.001
*
Endoscopic procedures include balloon dilation in three (60.00%) patients, papillary sphincterotomy resulting in duodenal perforation and death in one (20.00%) patient and plastic stent in one (20.00%) patient, and the difference was not significant (P ¼ 0.449).
cases, and approximation of medial side of ducts to each other to provide a new common duct for anastomosis in six (25.00%) cases and ligation of the aberrant right hepatic duct without any consequences in one (4.17%) case. There was no significant difference (P ¼ 0.105). A good result on the first attempt was achieved in 99 of 101 patients with direct suture repair (98.02%, success rate). Biliary stricture was developed in three (42.86%) patients, which was successfully managed by rehepaticojejunostomy in one patient. In the second patient, we could not find any duct at the hilum for rehepaticojejunostomy, so we performed segment three cholangiojejunostomy, which was unsuccessful, and the patient died postoperatively. The third patient who developed biliary stricture 12 mo after reconstruction was referred for radiologic balloon dilation, which unfortunately was unsuccessful and the patient died. The median time for development of stricture after hepaticojejunostomy was 10 (range, 6e12 mo) mo. Overall, the ultimate success rate for direct suture technique was 96.03% (97 of 101 cases). The outcome of direct suture technique is shown in Table 3. Totally, four (3.23%) mortalities occurred in direct suture repair: two (50.00%) early postoperative mortalities due to intraperitoneal sepsis and two (50.00%) late mortalities due to biliary stricture and recurrent cholangitis after
hepaticojejunostomy. Also, nine (7.26%) mortalities observed after nondirect repair. These patients were operated on for bile peritonitis using open drainage of the hilum (9 of 34 [26.47%] bile peritonitis were expired). Male gender and advanced age were associated with higher rate of mortality (Table 4). On the whole, 111 patients are still alive with overall success rate of 89.52% with a mean follow-up of 78 38 mo (2e230 mo), and 13 patients died (mortality rate of 10.48%).
Discussion In our study, the injuries were initiated by open cholecystectomy in 81 (65.32%) patients and laparoscopic cholecystectomy in 43 (34.68%) patients. Owing to novelty of laparoscopic surgeries in our institution, the overall rate of laparoscopy and the rate of laparoscopic-induced bile duct injuries were lower than that of open procedures. Most iatrogenic injuries to major bile duct during cholecystectomy are not recognized during the operation, rather may appear several days or weeks later as a bile peritonitis, biliary fistula, or progressive jaundice.14 Approximately one fourth of all major bile duct injuries are noted at the time of operation. More than three quarters of iatrogenic major bile duct injuries remain unrecognized during
Table 3 e The outcome of direct suture repair in 101 patients with a median follow-up time of 76 mo (range, 0.5e230 mo). Complication
No (%)
Procedure
Outcome
Bile stricture
3 (42.86)
Rehepaticojejunostomy in one patient Segment III cholangiojejunostomy in one patient Balloon dilatation of bile stricture under imaging guidance in one patient
Recovered Died Died
Generalized peritonitis (unknown origin)*
1 (14.29)
Irrigation and peritoneal drainage
Recovered
Hemorrhagic shock due to falciform ligament bleeding
1 (14.29)
Ligation of bleeding points with suture
Recovered
Postoperative intraperitoneal sepsis
2 (28.57)
Medical treatment
2 died
P value *
0.666
d
This patient had a liver abscess which was drained simultaneously with hepaticojejunostomy.
d
maddah et al iatrogenic injuries of the extrahepatic biliary system
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Table 4 e Distribution of mortality in each factor. Mortality
Expired
Survived
Total
P value
Type of operation Laparoscopy
4 (9.30%)
39 (90.70%)
43 (34.68%)
Open
9 (11.11%)
72 (88.89%)
81 (65.32%)
62.15 þ 12.92
45.38 þ 13.06
47.18 þ 13.99
Peritonitis
9 (26.47%)
25 (73.53%)
34 (27.42%)
Nonperitonitis
4 (4.44%)
86 (95.56%)
90 (72.58%)
Age (y)
0.996 <0.001
Presentation 0.001
Gender Male
6 (20.00%)
24 (80.00%)
30 (24.19%)
Female
7 (7.45%)
87 (92.55%)
94 (75.81%)
13.7 þ 4.83
20 þ 7.00
19.34 þ 5.92
<0.001
0.011
Time of injury recognition for bile peritonitis (d)
0.107
Gender in relation to bile peritonitis Male
5 (71.43%)
2 (28.57%)
7 (20.59%)
Female
4 (14.81%)
23 (85.19%)
27 (79.41%)
Age in relation to bile peritonitis (y) Male
63.6 5.5 (range, 47e80)
Female
60.6 þ 6.7 (range, 35e75)
the operations.15,16 However, in our series, only 19% (23 cases) of injuries were discovered at the time of cholecystectomy. The mean time for delayed recognition of injury in our series was 44.9 d. This is in contrast with other reported series with mean range of 12 and 16 d delay in recognition of injuries.10,17 Because of missing data, we cannot precisely justify the long delay in diagnosis of injury. However, it may be due to less severe injuries. The mean time of injury recognition for bile peritonitis in the dead patients was 13.7 d in contrast to 19.5 d in survivors. This is in conflict with the common sense that with earlier diagnosis the better prognosis is expected in the bile peritonitis patients. We assume that this increased mortality is probably due to bacterial peritonitis or physiologic state of the dead patients that worsened the condition of patient which mandates the physician to recognize the diagnosis of bile peritonitis earlier. Jaundice and cholangitis were the most common presenting manifestations in the present study (51.6%), followed by bile peritonitis (27.4%) and external fistula (20.9%). In a study by Pitt et al. 16 on 106 patients with postoperative bile duct injury, 77% of patients became jaundiced, and an external biliary fistula or bile peritonitis occurred in 14% and 43% of their patients, respectively. The localization of a bile duct stricture is of highest importance not only for proper management but also to determine the prognosis. There is a variety of classification systems developed to elucidate bile duct injuries with regard to anatomy. Bismuth developed a classification of bile duct strictures based on the anatomic patterns of involvement.6 Strasberg modified the original Bismuth classification into a more comprehensive system, which we chose for defining the anatomy of bile duct injuries. In Glenn’s report of 100 biliary tract injuries after open cholecystectomy, the most common site of injury was the cystic duct-common hepatic junction (58%).18 The most common site of injury in our study was transection in the
hilum (in the rate of 42.7%), which was in accordance with type E3 injuries in the Strasberg classification. The purpose of surgical repair in biliary tract injuries is to restore a durable bile conduit and to prevent both short-term and long-term complications, such as stricture and cholangitis.1 If the injury to the bile duct is recognized during cholecystectomy, it is then quite tempting to attempt a complex repair. The surgeon should assess the situation in terms of his own ability to deal with the problem. The surgeon should not underestimate the emotional impact of these injuries on his or her ability to perform definitive reconstruction. The surgeon should not also hesitate to ask for assistance from a more experienced surgeon, or it may be apt to provide external biliary drainage by means of proximal intubations and then refer the patient for definitive management to a center having expertise in such complex problems.14,19 The most favorable management is dependent on the timing of recognition of injury, the extent of bile duct injury, the patient’s condition, and the availability of experienced hepatobiliary surgeons.20 Bile peritonitis is the most crucial and potentially fatal consequence of the bile leakage.21 When septic bile peritonitis is present, laparotomy is indicated without further investigations.22 In this situation, because of bile ducts collapse and extreme staining of the tissues with bile, a definitive repair is scarcely possible. The goal then should be open drainage. The definitive reconstruction may be delayed until a subsequent date. In some patients, we performed multiple irrigation and drainage procedures. Mathews and Blumgart 14 suggested that the open drainage may be carried out through a mobilized Roux-en-y loop of jejunum with the open drainage tube simply being led in a transjejunal fashion to the exterior. Such a procedure permits initial control, and most often inevitably requires reoperation for bile duct stenosis.3
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j o u r n a l o f s u r g i c a l r e s e a r c h 1 j u n e 2 0 1 7 ( 2 1 3 ) 2 1 5 e2 2 1
In this situation, we preferred open drainage and late biliary reconstruction as needed. In construction of hepaticojejunostomy, few points should be considered. The criteria necessary for a successful biliary tract reconstruction have been listed by Rodney Smith as making the largest possible stoma, accurate apposition of mucosa to mucosa at all points around the stoma and an adequate blood supply.23 Mucosa to mucosa apposition is a basic requirement for obtaining long-term anastomotic patency, and all efforts should be made to reach this goal.24 For better apposition of mucosa to mucosa anastomosis, Breach et al. 25 advocated using a loop on the mucosa stitch to apply jejunal mucosa directly to the ductal mucosa. Considerable questions regarding the use of internal stenting and the optimal time for stenting of reconstructive procedure, whether decreases the stricture formation still remain unanswered. Some authors are skeptical about the value of stent, and rarely use transanastomotic splinting, however, they obtained good results.18,20,26 Bismuth et al. reported 123 patients with benign diseases who underwent Roux-en-y hepaticojejunostomy. In no instance was a stent used; only one instance of anastomotic stenosis was observed during a follow-up study averaging 5.5 y.26 On the other hand, several investigators feel strongly that stents are beneficial and claim that avoiding using stents may lead to recurrent cholangitis.17 They noted that it provides an adequate biliary drainage in the postoperative period and allows irrigation with sterile water to keep the bile passage clear of debris and cholangiograms are easily performed through the tube.23 Prolonged patency could also be expected in case of formation of collagen scar.27 Some experienced surgeons have advocated leaving splints in place for months to 2 y or until they become occluded.25 However, some authors believe that the best results appeared to be achieved in those patients who are intubated for 1 to 3 mo. The beneficial use of a tube deteriorates with prolonged use (longer than 3 mo) because of inflammation caused by a foreign body.27 In constructing hepaticojejunostomy when the lumen of anastomosis seems to be <1 cm, we usually use a transanastomotic stent which passes retrograde from the ducts out through the surface of the liver inside the Roux limb. The transhepatic tube was connected to external drainage until day 10 after surgery when cholangiography was performed. If no leakage was detected, the tube was closed and left in place then was removed after 6 wk. Although the short-term consequences of major bile duct injury and stricture are significant, it is the long-term outcome after repair that serves as the primary determinant of resolution of the complications. Lillemoe et al. 12 described the outcome of 156 patients after surgical reconstruction for bile duct strictures with a mean follow-up of 57.5 mo which showed overall success rate of 90.8% and one case of mortality due to pulmonary embolism. Pitt et al. 16 reported that by 3 y after a repair, only two-thirds of the patients who eventually had a recurrent stricture returned for reoperation, and even 5 y after operation for benign postoperative stricture, only 80% of recurrences occurred. Another
analysis underscores the need for prolonged follow-up in determining the results of surgery in these patients, so close surveillance for at least 5 y is mandatory after a stricture repair.19 In this study, the average follow-up period was 78 mo with a success rate of 98% with direct suture techniques at first attempt of reconstruction and ultimately a good result in 96% patients during this period. In this study, we found three biliary strictures of 101 cases of direct suture technique. The mean time for development of stricture was 10 mo after biliary reconstruction. The overall mortality rate in our study of patients was 11.5% (13 patients). This mortality rate is similar to other reports that have noted an early mortality rate ranging from 11%e18% in severely ill patients.10 Factors affecting mortality in our series were advanced age, male gender, and presentation with bile peritonitis (Table 4). Considering the introduction of laparoscopy in the last decade in Iran, in our study, there has been a high proportion of open surgery versus laparoscopic procedure, so we cannot compare biliary tract injuries in terms of the two surgical approaches. It can be acknowledged as a limitation of our study.
Conclusion The incidence of iatrogenic bile duct injuries has recently increased and has been associated with increased use of laparoscopic cholecystectomy worldwide. It is essential to be careful in the proper visualization of the surgical area and the identification of structures before ligation or transection to decrease the risk of bile duct injuries during surgery. When biliary injury develops, early recognition and appropriate treatment are of highest importance. Early and appropriate treatment allows avoidance of serious complications in patients with iatrogenic bile duct injuries. After bile duct repair, patients require long-term and careful postoperative observation because of the possibility of biliary anastomosis stricture.
Acknowledgment The results described in this article formed part of a thesis submitted by the third author to the Mashhad University of Medical Sciences for a postgraduate degree in general surgery. The study was supported by the Vice Chancellor for Research of Mashhad University of Medical Sciences (grant number: 920457). There was no funding obtained for the article. Authors contributions: Abdollahi Abbas, Maddah Ghodratollah, Rajabi Mashhadi Mohammad Taghi performed the conception and design. Abdollahi Abbas, Maddah Ghodratollah, Rajabi Mashhadi Mohammad Taghi contributed to analysis and/or interpretation of data. Maddah Ghodratollah, Rajabi Mashhadi Mohammad Taghi, Abdollahi Abbas, Parvizi Mashhadi Mehdi performed the data. Maddah Ghodratollah, Abdollahi Abbas, Parvizi Mashhadi Mehdi, Hassanpour Masoumeh wrote the article. Maddah Ghodratollah, Rajabi Mashhadi Mohammad Taghi, Abdollahi Abbas, Parvizi Mashhadi Mehdi, Jabbari Nooghabi Mehdi, Hassanpour Masoumeh
maddah et al iatrogenic injuries of the extrahepatic biliary system
performed the critical revision of data. Maddah Ghodratollah, Abdollahi Abbas, Jabbari Nooghabi Mehdi, Hassanpour Masoumeh performed the final approval. Jabbari Nooghabi Mehdi performed the statistical analysis. Maddah Ghodratollah, Abdollahi Abbas took the overall responsiblity.
Disclosure The authors declare no conflicts of interest.
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