Endoscopic sphincterotomy associated cholangitis in patients receiving proximal biliary self-expanding metal stents

Shanghai, China

Endoscopic sphincterotomy associated cholangitis in patients receiving proximal biliary self-expanding metal stents

Hui Zhou, Lei Li, Feng Zhu, Sheng-Zheng Luo, Xiao-Bo Cai and Xin-Jian Wan

Shanghai, China

BACKGROUND:Endoscopic biliary stent placement during the procedure of endoscopic retrograde cholangiopancreatography (ERCP) is preferred to provide biliary drainage for unresectable malignant biliary obstruction. There is considerable controversy over the use of endoscopic sphincterotomy (ES) prior to stent placement. This study aimed to determine whether ES before intraductal self-expanding metal stent (SEMS) placement affects the clinical outcome and complications in patients with proximal malignant obstructive biliary diseases.

METHODS:In a prospective randomized controlled trial, 82 patients with inoperable malignant biliary strictures were randomly assigned to biliary stenting groups with or without ES. Resolution of jaundice and the incidence of complications including acute cholangitis, pancreatitis and stent occlusion within 6 months were evaluated.

RESULTS:SEMSs were successfully deployed in all patients, resulting in clinical and biochemical improvement of obstructive symptoms in both groups. The incidence of cholangitis was higher in the ES group than in the non-ES group (58.5% vs 31.7%,P=0.015). The interval between stent placement and the first acute cholangitis was much shorter in the ES group than in the non-ES group (P=0.024). The use of ES increased the incidence of cholangitis (P=0.004, risk ratio, 8.196). The rate of post-ERCP pancreatitis after stent placement was greater in the non-ES group than in the ES group (31.7% vs 9.8%,P=0.014). No significant differences were found in the rate of restenosis and the mortality rate between the two groups.

CONCLUSIONS:ES prior to intraductal SEMS placement was associated with an increased incidence of acute cholangitis. ES should be carefully evaluated prior to its use in patients with proximal malignant obstructive biliary diseases.

(Hepatobiliary Pancreat Dis Int 2012;11:643-649)

sphincterotomy; biliary obstructions; endoscopic retrograde cholangiopancreatography; cholangitis; pancreatitis

Introduction

The prognosis of malignant biliary obstruction caused by metastatic cancer, cholangiocarcinoma, pancreatic adenocarcinoma, or gallbladder carcinoma is very poor.[1]Only 20% of the patients are suitable for surgical resection at the time of diagnosis.[2]Endoluminal palliation can resolve jaundice, relieve pain, and improve the quality of life of patients with inoperable malignant obstructive biliary diseases.[3-5]This procedure is less invasive and more cost-effective than surgical decompression approaches. Selfexpanding metal stent (SEMS) placement in the process of endoscopic retrograde cholangiopancreatography (ERCP) is preferred to provide biliary drainage for patients with predicted survival ＞6 months.[6-9]

Currently, there is controversy over the use of endoscopic sphincterotomy (ES) before the placement of biliary stents. Endoscopists who prefer ES have found that it may facilitate deep cannulation during difficult ERCP,[10]reduce resistance to the passage of stents, improve the final stent diameter, and reduce the occurrence of pancreatitis.[11,12]However, ES has been reported to be independently associated with an overall postoperative complication rate of 11.7% (i.e., bleeding, pancreatitis, perforation, and cholangitis), even when performed by experienced endoscopists.[13-15]Also, ES increases the operative time and cost. Currently, thereare no guidelines regarding whether ES should be performed when a biliary stent is placed.

Several studies[3,9,11,14]have reported mixed findings on the use of ES in patients who underwent transpapillary stent placement because of malignant biliary strictures. As such, it remains unclear whether patients with proximal malignant biliary strictures who receive nontranspapillary SEMS placement benefit from the application of ES. The present prospective randomized control trial was designed to analyze the clinical outcomes and incidence of acute cholangitis and acute pancreatitis during a 6-month follow-up period in patients who did or did not undergo ES immediately before SEMS placement in the process of ERCP.

Methods

Eligibility criteria and randomization

From June 2006 to June 2009, 82 inpatients with unresectable proximal biliary obstruction, diagnosed as hilar cholangiocarcinoma, choledochus carcinoma, gallbladder carcinoma or pancreatic adenocarcinoma, were enrolled in the study. The study protocol was approved by the Ethics Committee of Shanghai First People's Hospital of Shanghai Jiaotong University. The diagnosis and poor prognosis of the patients were established by a combination of clinical, laboratory and imaging methods (computed tomography, magnetic resonance imaging, and/or endoscopic ultrasound), biopsy or brush cytology, and age. Surgical consultation was obtained to assess if the tumor was resectable or unresectable. Written informed consent was obtained from all patients.

The exclusion criteria included patients who had already undergone ES or stent placement, as well as those with previous Billroth II resection (since ERCP and ES in these patients are difficult), severe coagulation abnormalities, disturbance in liver and renal function, chronic wasting disease and other biliary tract diseases. Those whose tumors involved the distal common bile duct (CBD; distal CBD defined as the lower 2 cm of the CBD) and were identified to be of porta hepatic tumor type IV were also excluded.

The patients were randomized after successful cannulation of the bile duct according to a computergenerated randomization list to one of the two groups. In the ES group (41 patients), ES was performed before SEMS deployment. The non-ES group (41 patients) received SEMS placement without ES.

Interventions and stent deployment

After diagnosis, all patients underwent operative ERCP with a duodenoscope (JF 140, Olympus) by one of two experienced endoscopists. The ERCP was performed according to a standardized protocol in both groups. All patients were treated by intravenous administration of broad-spectrum antibiotics during the procedure. The bile duct was cannulated, and the presence and position of biliary strictures were confirmed cholangiographically. For patients assigned to the ES group, the cannula was exchanged for an Ultratome (Boston Scientific, Natick), and a 10- to 15-mm sphincterotomy was performed electrosurgically. Then a metallic biliary stent was inserted over a standard 0.035-inch guide-wire, and the distal tip of the stent was situated in the bile duct, not protruding into the duodenum. For patients in the non-ES group, the cannula was removed, and a metallic biliary stent was inserted through the native papilla. Then the stent was passed through the strictures and positioned above the main duodenal papilla. For hilar cholangiocarcinoma, the proximal tip of the stent was placed in the stricture of the intrahepatic bile duct. For upper cholangiocarcinoma, the right hepatic duct was the common choice if the stent was to be placed in the hepatic bile duct. Both tips of the stents were positioned 2 cm immediately proximal and immediately distal to the stricture. Uncovered 10-mm-diameter SEMSs were used in this study [Micro-Tech (Nanjing) Co., Ltd., China]. The success of technique was evaluated as endoscopic and cholangiographic views of a stent in a satisfactory position in the stenosed duct and good drainage of bile from the bile duct into the duodenum. The patients were observed for at least one week after the procedure.

In the follow-up period, stents were not replaced routinely and the patients were treated if occlusion of the stent or cholangitis developed. After treatment with antibiotics for 3 days, if patients with acute cholangitis did not improve and cholangitis was due to suspected occlusion of the stent, ERCP was repeated. A second stent was indicated for placement if a biliary obstruction occurred.

ERCP database and definition of events

The demographics of the patients, indications for SEMS placement, length and position of biliary stricture and stent, presence or absence of ES, clinical outcomes (complete blood count, biochemical tests of liver function, patency interval and occlusion of stent), infectious complications, and a second ERCP procedure within 6 months were recorded for later analysis.

For procedural complications as described by Cotton et al,[16]we focused on the incidence of acute cholangitis. Other post-ERCP pancreatitis (PEP), occlusion andpatency interval were also evaluated. Acute cholangitis was confirmed by clinical symptoms such as body temperature ＞38 ℃, leukocytosis, and chills in the absence of another explanation, or on ultrasound and CT findings. PEP was diagnosed if the patient had typical abdominal pain associated with serum amylase or lipase levels three times the upper limits of normal＞24 hours after the procedure, which required treatment for ＞2 days. Patency interval was defined as the period between the first SEMS placement and the occurrence of stent occlusion. Occlusion was considered in patients with jaundice.

Follow-up

Follow-up data subsequent to SEMS placement for all patients were logged prospectively into an ERCP database. The therapeutic effects and incidence of complications (occurring within 6 months, from the date of ERCP until the end of the study or death) were recorded and assessed. A complete blood count and biochemical tests of liver function were monitored before ERCP, daily in the two days immediately after ERCP and evaluated in the following 1 week and 1, 3, and 6 months.

Statistical analysis

The data obtained were transferred into SPSS 16.0 for Windows (SPSS Inc., Chicago, IL., USA) for statistical analysis. Multivariate analysis was made to compare total bilirubin level, alkaline phosphatase (ALP), and white blood cell (WBC) count before and after stent placement between patients with ES and those without ES before SEMS placement. The incidence rate of infections and mortality rate were analyzed using the Chi-square test or Fisher's exact test. The survival, stent patency and interval between stent placement and the first occurrence of acute cholangitis were calculated according to the Kaplan-Meier method. Logistic regression was used to analyze the factors associated with the incidence of cholangitis. For other statistical analysis, the unpaired Student'sttest was used to compare the results from the two groups. Results were expressed as either percentages or mean±SD. APvalue of ＜0.05 was considered statistically significant.

Results

Patient characteristics

There was no difference between patients with and without ES in terms of age, gender, total bilirubin level, ALP, and WBC count before treatment (Table 1).Indications for non-transpapillary SEMS placement were biliary obstruction caused by hilar cholangiocarcinoma, choledochus carcinoma, gallbladder carcinoma and pancreatic adenocarcinoma (Table 1). According to the Bismuth classification,[4]34 patients with hilar strictures were diagnosed as having tumors of types I, II or III. No differences were observed in the length of a stent or the distance from the distal tip of the stent to the papilla between the two groups (Table 2).

Table 1.Patient characteristics

Table 2.Anatomical and procedural data for patients undergoing SEMS placement

Patient outcomes and complications

Fig. 1.Total bilirubin (A), ALP (B) and WBC count (C) before the procedure and post-treatment in the 2 groups after SEMS placement.

Fig. 2.A.Kaplan-Meier life-table analysis of the interval between stent placement and the first acute cholangitis (P=0.024).B.Kaplan-Meier life-table analysis of the stent patency (P=0.700).C.Survival rates of patients in the 2 groups (P=0.756).

Stents were successfully deployed in all 82 patients. There was no procedure-related mortality. The obstructive symptoms, liver function and jaundice of the patients were improved in the ES and non-ES groups (Fig. 1). The total bilirubin levels at 1 week, and 1, 3 and 6 months after the procedure declined in the two groups compared with those before the procedure (P＜0.001; Fig. 1A). Other tests of liver function showed similar changes after the procedure in the ES and non-ES groups. Serum ALP levels decreased at every time point after the procedure, compared with that before SEMS placement (1 week, and 1, 3 and 6 months after the procedure versus before the procedure in the two groups,P＜0.001, Fig. 1B). WBC count in both groups showed similar changes (except for 1 week versus before the procedure in the ES group (P=0.03, all other times after the procedure versus before the procedure in both groups,P＜0.001, Fig. 1C). Comparing the effectiveness of the procedure between the two groups showed that there was no significant difference in liver function and WBC count after the procedure between the ES and non-ES groups (total bilirubin level,P=0.402, Fig. 1A; ALP,P=0.188, Fig. 1B; WBC count,P=0.292, Fig. 1C).

No patients were lost to follow-up in this period. The clinical outcomes and complications such as infections after ERCP are summarized in Table 3. In the ES group, 24 patients suffered from acute cholangitis and 4 from acute pancreatitis. Two patients had complications of acute cholangitis and pancreatitis during the follow-up period. In the non-ES group, 13 patients suffered from acute cholangitis and 13 from acute pancreatitis. Four patients had both acute cholangitis and pancreatitis. Comparing complications between the two groups showed the incidence of cholangitis was lower in the non-ES group than in the ES group (P=0.015, Table 3), whereas the incidence of pancreatitis was higher in the non-ES group than in the ES group after SEMS placement (P=0.014, Table 3). The interval between stent placement and the appearance of acute cholangitis in the ES group was much shorter than that in the non-ES group (P=0.024, Fig. 2A). The PEP of the patients in our study was recognized as mild according to the Cotton criteria.[16]All patients with pancreatitis in the two groups were treated successfully with conservative therapy. However, in patients with acute cholangitis, 5 (12.2%) in the ES group and 4 (9.8%) in the non-ES group, who were found to have stent occlusion, were given an additional stent endoscopically (Table 3). No difference was found in the stent patency between the two groups (Fig. 2B). Two patients in the ES group and 3 in the non-ES group died of acute cholangitis or tumor development during the follow-up period (Fig. 2C). No significant difference was detected in the mortality rate between the two groups (Table 3).

Table 3.Outcomes and complications of stent placement by presence or absence of sphincterotomy

The risk factors for acute cholangitis included the distance from the end of the stent to the duodenal papilla (P＜0.001), the location of stricture of the bileduct (P＜0.001), types of malignant diseases (P＜0.001), and use of ES (P=0.007). Multiple logistic regression analysis of these risk factors showed that the application of ES (P=0.004; risk ratio, 8.196) significantly increased the incidence of cholangitis.

Discussion

In the current study, ES before SEMS placement in patients with proximal malignant biliary obstruction did not improve the symptoms of jaundice but increased the risks and complications of acute cholangitis.

Studies[4,5,17-21]reported the effectiveness of endoscopic biliary stent placement in the management of malignant biliary obstruction. The main advantages of SEMS over plastic stent in the palliation of malignant biliary strictures include longer patency and greater complicationfree survival.[22-24]The present study demonstrated that SEMS placement relieved the obstructive symptoms in patients with proximal malignant biliary diseases. The improvement of jaundice and cholangitis through biliary drainage was recorded in both groups during the followup for 6 months.

ES is commonly performed to remove bile duct stones. Routine ES prior to stent insertion is controversial. Reports[25,26]have shown that ES can facilitate the placement of stents through malignant and benign biliary strictures, produce better biliary drainage, and reduce the risk of PEP.[11,12]Still others have indicated that the risks of ES might outweigh any potential benefit for the patient[27,28]because of procedure-related complications.[12-15]In this study, SEMSs were placed in the upper bile ducts of patients with proximal biliary strictures. The placement of the stent above the intact sphincter of Oddi was reported to be associated with adequate stent patency and a lower occlusion rate.[29]ES may reduce resistance to passage of the stent and reduce damage to the papilla caused by PEP from SEMS insertion. Hence endoscopists prefer to perform ES before non-transpapillary SEMS insertion.[30,31]

In the study SEMS placement in the non-ES group was technically successful as reported elsewhere.[3,12,32,33]The patients who underwent ES had a high risk of acute cholangitis than those who did not. In the follow-up period, the incidence of acute cholangitis after SEMS placement was doubled in the two groups. Analysis of the multiple risk factors demonstrated that the application of ES may significantly increase the incidence of cholangitis.

In our study, the incidence of PEP was higher in the non-ES group than that reported elsewhere.[34]However few studies were performed to evaluate the incidence of pancreatitis when a large-diameter SEMS was placed in the bile duct. We thought that procedural techniques may be partially responsible for the high risk of PEP in our study. PEP occurred within the first 24 hours after SEMS placement and was successfully treated conservatively with antibiotics. We noted that using ES or not did not reduce the incidence of stent occlusion and mortality. This may be due to the small sample size of our study.

The effect of ES in SEMS placement associated with the incidence of acute cholangitis remains unclear. According to the report by Cotton et al,[16]lack of drainage is one of the etiological factors for acute cholangitis. For transpapillary stent placement in patients with distal CBD strictures, ES could expand the stent diameter for a better drainage. This factor can be dismissed because of the non-transpapillary SEMS deployment. Stent placement above the sphincter of Oddi might prevent the migration of bacteria and the deposition of organic material in the stent.[35]In fact, the sphincter of Oddi acts as an effective mechanical barrier to bacterial invasion from the duodenum.[36]The breached sphincter in patients with ES may lead to the ascending bacterial colonization in the biliary tract[37]and result in duodenal juice reflux, which may stimulate the inflammatory reaction of epithelial cells of the bile duct. However, endoscopic management such as ES may be associated with persistant clinical infection. In the long-term effects of ES other than stent occlusion, sphincterotomy stenosis may contribute to the obstruction of the bile duct.

In conclusion, ES before intraductal SEMS placement is associated more frequently with cholangitis in patients with proximal malignant obstructive biliary diseases. Further studies in a larger number of patients are necessary to confirm the lack of application of ES before stent placement.

Contributors:WXJ designed the research. ZH, LL, ZF, LSZ and CXB performed the research. ZH analyzed the data and wrote the paper. All authors contributed to the design and interpretation of the study and to further drafts. WXJ is the guarantor.

Funding:None.

Ethical approval:The study protocol was approved by the Ethics Committee of Shanghai First People's Hospital of Shanghai Jiaotong University.

Competing interest:No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

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Accepted after revision June 6, 2012

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February 27, 2012

10.1016/S1499-3872(12)60239-2)

Author Affiliations: Department of Gastroenterology, Shanghai First People's Hospital, Shanghai Jiaotong University, Shanghai 200080, China (Zhou H, Li L, Zhu F, Luo SZ, Cai XB and Wan XJ)

Xin-Jian Wan, MD, Department of Gastroenterology, Shanghai First People's Hospital, Shanghai Jiaotong University, 100 Haining Road, Shanghai 200080, China (Tel: 86-21-63240090; Fax: 86-21-63240825; Email: Wanxj99@163.com)

? 2012, Hepatobiliary Pancreat Dis Int. All rights reserved.

doi: 10.1016/S1499-3872(12)60238-0