current management of postoperative complications and benign biliary strictures

Gastrointest Endoscopy Clin N Am

13 (2003) 635–648

Current management of postoperative

complications and benign biliary strictures

Guido Costamagna, MD, FACG*,Saumil K. Shah, MD, DNB, DM, DNB, Andrea Tringali, MD

Digestive Endoscopy Unit, Department of Surgery, Catholic University, Largo A. Gemelli 8,

Rome 00168, Italy

Postoperative bile duct injuries may occur after any kind of surgical

procedure involving the biliary tract. Such injuries, however, are most frequent

following cholecystectomy and biliary anastomosis (eg, after liver transplan-

tation). Although laparoscopic cholecystectomy (LC) results in a shorter hos-

pital stay, faster recovery, lower overall morbidity, and a better abdominal

cosmetic outcome, the rate of bile duct injuries is two to six times higher than

with open cholecystectomy (OC) [1,2]. At least one third of these injuries are

not related to inexperience but reflect fundamental errors in the technique of

LC [3]. Compared with OC, biliary injuries sustained during LC present earlier,

are often associated with persistent bile leaks, and are usually high injuries (ie,

injuries usually located at the common hepatic duct or at the hilum) (Fig. 1A)

[4]. Unfortunately, biliary injury is seldom recognized during surgery; symp-

toms appear most often in the early postoperative course or months or years

after surgery.

Biliary complications are also a common cause of morbidity following or-

thotopic liver transplantation (OLT). Biliary complication after OLT occurs in one

of every six patients, usually within the first 3 months after transplantation.

Although bile duct leaks and strictures are the most common complications,

sphincter of Oddi dysfunction, hemobilia, and biliary obstruction from stones,

sludge, or casts have also been described [5]. Leaks usually present much earlier

than obstructive pathologies.

1052-5157/03/$ – see front matter D 2003 Elsevier Inc. All rights reserved.

doi:10.1016/S1052-5157(03)00103-X

* Corresponding author.

E-mail address: [email protected] (G. Costamagna).

Fig. 1. (A) Endoscopic retrograde cholangiopancreatography showing a leak from the cystic duct

stump after laparoscopic cholecystectomy. (B) Check cholangiogram through the nasobiliary drain

48 hours after endoscopic sphincterotomy: the leak is no longer visible.

G. Costamagna et al / Gastrointest Endoscopy Clin N Am 13 (2003) 635–648636

Bergman and colleagues [6] described four types of postoperative bile

duct injuries:

Type A: cystic duct leaks or leakage from aberrant or peripheral hepatic radicles

Type B: major bile duct leaks with or without concomitant biliary strictures

Type C: bile duct strictures without bile leakage

Type D: complete transection of the duct with or without excision of some

portion of the biliary tree

Although such iatrogenic injuries are initially evaluated with ultrasonography,

computed tomography (CT) scan, cholescintigraphy [7], or magnetic resonance

cholangiopancreatography (MRCP) [8], an endoscopic retrograde cholangiopan-

creatography (ERCP) or a percutaneous transhepatic cholangiography (PTC) needs

to be performed eventually for therapy. A cholangiogram is of utmost importance

for accurate anatomic depiction and to classify the type of injury so as to

plan therapy.

G. Costamagna et al / Gastrointest Endoscopy Clin N Am 13 (2003) 635–648 637

Surgery has been the mainstay of therapy for such iatrogenic biliary injuries.

Surgery, however, is associated with considerable morbidity and mortality [9,10].

Recent experience with endotherapy has been encouraging [11–17]. Percutaneous

transhepatic techniques are usually reserved for failed endoscopic procedures.

For purposes of the present discussion, postoperative bile duct injuries have

been arranged in two groups: bile leaks and bile duct strictures.

Postoperative bile leaks

The reported incidence of biliary leaks following OC is 0.5% or less and

following LC is 1.1% [18]. Rates of intraoperative complication and conversion

to open surgery were greater among patients who developed leaks [19]. Bile leak

into the peritoneal cavity or externally through a drain positioned at surgery may

have multiple origins according to the type of surgery performed. The following

are the major causes of occurrence of leak:

� Cholecystectomy (open or laparoscopic)

1. Cystic duct stump leak caused by misplacement or displacement of clips

or ligature, a tear in the remnant proximal to the clip, or a necrotic duct

remnant that fails to close because of an ongoing necroinflamma-

tory response

2. Common bile duct (CBD) injury with subsequent leakage following er-

rant clip placement, inadvertent electrocautery or laser burn, excessive

traction on the cystic duct, or inadvertent transection

3. Injury of a sectorial, segmental, or subsegmental duct in the setting of an

anatomic variation of the main biliary confluence

4. Leakage from the gallbladder bed caused by transection of cystohepatic

ducts of Luschka
� Surgery involving the CBD
1. Injury to the CBD or to a major branch at the main confluence

2. Leakage from the choledochotomy

3. Leakage from a duct-to-duct anastomosis (as in liver transplantation)

4. Leakage from a biliodigestive anastomosis
� Hepatic surgery
1. Injury to the CBD or to a major branch at the main confluence

2. Leakage from a ligated or clipped hepatic radicle

3. Leakage from intrahepatic bile ducts at the hepatic surface after liver

resection

4. Leakage from intrahepatic bile ducts at the hepatic surface after peri-

cystectomy for hydatid cyst

5. Leakage from intrahepatic bile ducts after surgery for hepatic trauma

A high index of suspicion allows early treatment. Patients with postoperative

bile leaks occurring from either open or laparoscopic surgery have a similar


presentation. Patients may present with malaise, nausea, vomiting, fever, ileus,

jaundice, abdominal pain, or right shoulder pain. Presence of bilious ascites or a

palpable biloma is extremely unusual [18]. Abnormalities in the hepatic profile

are noted, and the white blood cell count may be elevated.

Once the diagnosis of bile leak is established (evidence of external fistula,

radionuclide hepatobiliary scan documenting a leak, or the presence of a biloma at

ultrasound or CT examination), a confirmatory cholangiography is mandatory and

is best accomplished by ERCP [1,12,18,20]. Apart from providing precise

anatomic diagnosis, it allows therapy. PTC or MRCP should be reserved for

patients in whom ERCP fails technically or fails to show the intrahepatic biliary

anatomy because of proximal ductal disruption [18]. For interpretation purposes,

especially in the case of complex hilar lesions, ERCP is best performed with the

patient in the supine position. Doing so allows changing of the patient’s position

obliquely and thus substantially helps in identifying the anatomy of themain biliary

confluence and of the segmental intrahepatic ducts.

Apart from complete transection of the CBD (type D lesion), which is generally

an indication for reconstructive surgery (typically by Roux-en-Y hepaticojeju-

nostomy), an endoscopic therapeutic approach may be envisaged. Endotherapy

has been highly successful in the treatment of postoperative bile leaks [11–13,

15,17,21–24]. Binmoeller and colleagues [11] reviewed 77 cases of endoscopic

therapy reported before 1991 and found technical success in 95% and healing of

the leak in 82% of patients. Elimination of the transpapillary pressure gradient,

thus equalizing the bile duct and duodenal pressures and allowing flow of bile into

the duodenum [12], results in healing within 2 to 8 days [15]. The transpapillary

pressure gradient can be equalized by endoscopic sphincterotomy (ES) alone

[15,17], ES and stent [17] or nasobiliary drain (NBD) placement [25], and stent

[21,26] or NBD insertion alone [27] without preliminary ES (Fig. 1B). All

methods seem to be equally effective in facilitating the closure of the biliary leak

within a few days [6,11,12,21], and the endoscopic approach of choice remains

controversial. The authors’ experience over 13 years in 105 patients with

postoperative biliary leaks has also been excellent. They performed ES plus

NBD placement in 70 patients (68%), ES plus stent placement in 21 patients

(20.4%), and ES alone in 12 patients (11.6%). They achieved a success rate of

98% and had a complication rate of 2% without any mortality. They prefer to place

a NBD because serial cholangiograms can be performed, and a repeat endoscopic

procedure is avoided. If a stent is to be placed, a stent of 10 F or larger is preferred

to avoid early clogging. Endoscopic sphincterotomy followed by stone extraction

should be preferred when dealing with associated residual CBD stones (29% of

cases in the authors’ experience).

Each of these options has limitations, however. Endoscopic sphincterotomy is

associated with inherent immediate and long-term complications, stenting neces-

sitates a repeat procedure and can become clogged or can migrate, whereas a

NBD necessitates continued hospitalization, is uncomfortable for the patient, and

could be accidentally displaced. Recently, Marks and colleagues [28] docu-

mented significantly lower CBD pressures within 24 hours after injection of


botulinum toxin (Botox, 100 units) into the sphincter of Oddi; the lower pressures

persisted for 14 days. The authors have suggested its use for the treatment of

bile leaks.

For type B lesions, despite absence of a stricture, the authors prefer to insert at

least one 10-F or 11.5-F stent to bypass the site of injury and to re-establish a

good bilioduodenal flow. The secondary intent of stent placement is to prevent

the development of stricture at the site of the injured bile duct wall. For long

ductal rents, others have also preferred to place long stents across the leak site

[12,18]. Therapeutic success may be obtained in 71% to 79% of cases in this

setting [6,29,30]. Biliary stents have also been successfully used to reestablish the

continuity of disrupted sectorial or segmental branches at the level of the main

hepatic confluence [31] and for leaks from accessory bile ducts [18,32].

Percutaneous drainage of localized bile collections can be a useful adjunctive

therapy when the size or duration of the leak has produced significant intra-

abdominal fluid collection [6,12].

In conclusion, postoperative bile leaks are often amenable to endoscopic man-

agement with high success rates and minimal complications. Endoscopic sphinc-

terotomy with or without placement of drains or stents according to the site and

extent of injury in an individual patient must be considered as the first-line

treatment in all cases of postoperative bile leaks with very few exceptions. Botox

injection in the sphincter of Oddi seems interesting and requires further evaluation.

Postoperative bile duct strictures

Postoperative bile duct strictures occur in 0.2% to 0.5% of patients following

cholecystectomy and are often the result of direct surgical trauma from partial or

complete transection by clipping or ligation of the bile duct. Occasionally, the

stricture is caused by an ischemic insult of the biliary wall secondary to dissection

or thermal injury [14].

Bismuth [33] classified such benign strictures into five types:

Type 1: Low common hepatic duct (CHD) or bile duct (CHD > 2 cm) (Fig. 2A)

Type 2: Mid common hepatic duct (CHD < 2 cm) (Fig. 2B)

Type 3: Hilar stricture (Fig. 2C)

Type 4: Destruction of hilar confluence (right and left hepatic ducts separated)

(Fig. 2D)

Type 5: Involvement of right hepatic branch alone or with common duct

(Fig. 2E)

Greater distance from the hilar confluence along with early referral, good-

quality tissue of the proximal duct, and no previous repair are considered factors

associated with more favorable outcome after surgical reconstruction.

Although only 10% of postoperative strictures are suspected within the first

week after cholecystectomy, nearly 70% are identified within the first 6 months,

Fig. 2. Bismuth classification of postoperative bile duct strictures. (A) Type 1 stricture involving the

lower part of the common hepatic duct (CHD) or the common bile duct (CHD > 2 cm). (B) Type 2

stricture involving the midpart of the common hepatic duct (CHD < 2 cm). (C) Type 3 stricture at the

level of the main biliary confluence. (D) Type 4 stricture involving the main biliary confluence.

(E) Type 5 stricture involving the right hepatic duct or a right sectional branch (arrow) without

involvement of the common duct.


Fig. 2 (continued ).


and more than 80% are identified within 1 year of surgery. In the remaining

patients, presentation may be delayed for several years [34]. Patients present with

jaundice, recurrent cholangitis, abdominal pain, pruritus, bile duct stone formation,

and, occasionally, even secondary biliary cirrhosis. Liver biochemistry usually

shows evidence of cholestasis. ERCP or PTC needs to be performed after initial

evaluation with ultrasound, CT, or MRCP.

Traditionally, postoperative bile duct strictures have been managed surgically,

mainly by Roux-en-Y hepaticojejunostomy. Morbidity and mortality rates of

approximately 18% to 51% and 4% to 13%, respectively, [14,35–38] and rates of

stricture recurrence of 10% to 30% [39,40], requiring re-interventions that carry

even higher risk of recurrent strictures [41], have prompted attempts at alternative

therapies. In recent years, percutaneous and endoscopic techniques have been

developed to tackle such lesions.

Percutaneous therapy with balloon dilation of the stricture as a single modality

has been limited by the high recurrence rates of stricture [14,42]. One third of



patients experienced complications, and recurrent stenoses were noted in about

one fourth [43,44]. Reports from the John Hopkins Hospital documented a

success rate as low as 55% with significant hemobilia in 20% of patients [45].

Endoscopic treatment of postoperative bile duct stricture is often preferred

over percutaneous techniques, because it avoids the need for liver puncture and

because access to nondilated intrahepatic ducts is easier. Also, the endoscopic

approach is more comfortable for the patient and is safer in the presence of

cirrhosis, ascites, or coagulopathy.

All patients with postoperative bile duct strictures are amenable to a trial of

endoscopic management except those with complete transection or ligation of

the bile duct (Fig. 3). The advantage with endotherapy is that, if it fails, surgery

is still feasible, whereas hepaticojejunostomy makes future endotherapy difficult

if not impossible. The major disadvantage of endotherapy is the need for mul-

tiple procedures. Strictures at or above the main hepatic confluence are often

more challenging than strictures below the hepatic confluence. Endotherapy in-

volves temporary placement of plastic stents with or without preliminary hydro-

static balloon dilation. Balloon dilation is usually performed to a size 1- to 2-mm

larger than the downstream bile duct diameter. In most published experiences,

one or two 10- to 12-F stents were placed, with scheduled exchanges every 3 to

4 months for up to 1 year [14,46–48]. Successful stricture dilation has been

Fig. 3. ERCP showing complete transection of the common bile duct.


achieved in 74% to 90% of patients [3,14,49,50]. Bergman and colleagues [46]

followed patients for a median follow-up of 9.1 years and found stricture

recurrence in 20% of patients within 2 years of stent removal. A mean

follow-up of 42 months has shown a stricture recurrence rate of 17%, all

occurring in the first 30 months (mean, 3 months) after stent removal [47].

Endoscopic stenting and surgical bilioenteric anastomosis for benign biliary

strictures have been shown to have similar long-term success rates of around

80% [40,47,49]. Early complications occurred more frequently in the surgically

treated group, whereas late complications occurred only in the endoscopically

treated group [47].


Stricture at the choledochocholedochostomy anastomotic site is a major cause

of morbidity following OLT. Encouraging results have also been obtained

following endoscopic balloon dilatation or stent placement in patients with

anastomotic biliary strictures after OLT [21,22]. In 63% of patients, a single or

repeat balloon dilatation (8–11.5 mm) alone was sufficient [16]. Repeated

treatment was required more frequently for benign strictures complicating OLT

than for other surgical procedures [47].

To improve the results of endotherapy of postoperative bile duct strictures, the

authors systematically undertook a more aggressive approach based on the

Fig. 4. (A) Bile duct stricture (Bismuth type 2) after LC. (B) Five large-bore plastic stents have been

placed. (C) Disappearance of the stricture after removal of stents.


principle that placement of an increasing number of stents until complete

morphologic disappearance of the stricture would have better long-term patency

(Fig. 4) [51]. Endoscopic sphincterotomy was always performed because wide

access to the bile duct allowed insertion ofmultiple stents. Balloon stricture dilation

was performed whenever necessary. At each stent exchange (scheduled every

3 months), as many stents as possible were inserted, according to the tightness of

the stricture and to the downstream duct diameter. Forty-two of 45 patients

completed the protocol. There was no increase in early or delayed complication

rates. Complete morphologic disappearance of the stricture was obtained in

40 patients (89%) with a mean number of 3.2 ± 1.3 stents (range, 1–6 stents)

for a mean duration of 12.1 ± 5.3 months (range, 2–24 months). Two patients died

of unrelated causes on therapy. The remaining patients were followed for a mean of

48.8 months (range. 24 months–11.3 years). Thirty-nine of these 40 patients

remained asymptomatic and had normal biochemical and radiologic results. Such

an aggressive approach to endoscopic treatment with stents may improve long-term

results for patients with postoperative biliary strictures.



Long-term results with the use of metallic stents for such strictures have been

disappointing because patency is usually short term, and most stents eventually

obstruct [49,52].

The use of self-expanding metal stents is also not recommended. An

experimental study on pigs [53] showed inflammation, fibrosis, and intramural

abscess after removal of nitinol stents. The authors conclude that endoscopic

removal of self-expandable metal stents is not yet demonstrably reliable and safe.

Other endoscopic devices for the treatment of postoperative biliary strictures

are expected in the future. The development of bioabsorbable stents, removable

large-bore stents, or a stent that may be coated with steroids or chemotherapeutic

agents (such as coronary stents) could offer new possibilities for treatment.

In conclusion, an endoscopic attempt at management of postoperative bile

duct strictures should be undertaken as a first-line treatment in most instances. An

aggressive approach placing multiple stents improves results. Surgical recon-

struction should be considered for complete transection of the bile duct or when

endotherapy fails or stricture recurs.

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current management of postoperative complications and benign biliary strictures

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