Early Infectious Complications of Percutaneous Metallic Stent Insertion for Malignant Biliary Obstruction

Vascular and Interventional Radiology Original Research Sol et al. Stent Insertion in Biliary Obstruction Vascular and Interventional Radiology Original Research Yu Li Sol 1 Chang Won Kim 1 Ung Bae Jeon 1 Nam Kyung Lee 1 Suk Kim 1 Dae Hwan Kang 2 Gwang Ha Kim 2 Sol YL, Kim CW, Jeon UB, et al. Keywords: acute cholangitis, complications, infection, malignant biliary obstruction, percutaneous metallic stent DOI:10.2214/AJR.09.2474 Received January 29, 2009; accepted after revision June 12, 2009. Supported by Pusan National University research grant, 2008. 1 Department of Radiology, College of Medicine, Medical Research Institute, Pusan National University Hospital, 1-10, Ami-Dong, Seo-Gu, Busan 602-739, Republic of Korea. Address correspondence to C. W. Kim (radkim@hanafos.com). 2 Department of Internal Medicine, College of Medicine, Pusan National University Hospital, Busan, Republic of Korea. AJR 2010; 194:261 265 0361 803X/10/1941 261 American Roentgen Ray Society Early Infectious Complications of Percutaneous Metallic Stent Insertion for Malignant Biliary Obstruction OBJECTIVE. This study was designed to evaluate predisposing factors for early infectious complications after percutaneous metallic biliary stent insertion in patients with malignant biliary obstruction. MATERIALS AND METHODS. From August 1999 to June 2008, 215 consecutively registered patients with inoperable malignant biliary obstruction were treated with percutaneous placement of a metallic stent. The incidence of early infectious complications was evaluated. Sex, age, level of obstruction, type and number of stents, and stent position (across or above the main duodenal papilla) were retrospectively reviewed. The findings in patients with early infectious complications were compared with those in patients without early infectious complications. RESULTS. Infectious complications occurred within 30 days after stent placement in 14 of 215 (6.5%) patients. Univariate analysis showed a significant difference between the two groups with respect to nontranspapillary stent placement (p = 0.003). In the multiple logistic regression analysis, age, sex, level of obstruction, and type and number of stents were negatively associated with the development of early infectious complications (p > 0.05). CONCLUSION. Our study data showed that stent placement across the main duodenal papilla seemed to prevent early infectious complications after percutaneous metallic biliary stent insertion in patients with malignant biliary obstruction. I n patients with malignant biliary obstruction, percutaneous or endoscopic placement of a biliary stent has been widely used to manage the biliary obstruction and to improve and maintain quality of life [1 3]. Percutaneous insertion of stents has been established as the palliative treatment of choice, especially of patients with hilar strictures, because endoscopic drainage has higher rates of failure and complications [4 7]. One of the most common and serious complications after percutaneous biliary stent placement is infection, such as acute cholangitis and, which can impair quality of life [8 10]. Because of the risk of acute cholangitis, the decision to place a stent across the main duodenal papilla is controversial [11 13]. In addition, consensus has not been reached on whether a covered or an uncovered stent is more likely to induce acute cholangitis [14 18]. Many studies have been conducted to evaluate the risk of early infectious complications and late cholangitis after endoscopic biliary stent placement [13, 17, 19]. Few studies have described the occurrence of infectious complications within 30 days after percutaneous biliary stent placement [10, 14, 20]. The purpose of this study was to evaluate predisposing factors, such as type of stent (covered or uncovered) and stent position (across or above the main duodenal papilla), in the development of early infectious complications of percutaneous metallic biliary stent placement in patients with malignant biliary obstruction. Materials and Methods Patients From August 1999 to June 2008, percutaneous placement of metallic stents was attempted in 215 consecutively registered patients (120 men, 95 women; mean age, 66.5 years; range, 34 87 years) with unresectable malignant biliary obstruction. The institutional review board approved this retrospective study with a waiver of the requirement for informed consent. Clinical diagnoses were based on imaging findings after CT, MRI, ultrasound, or ERCP examinations. Follow-up clinical and radiologic findings after stent placement were AJR:194, January 2010 261

Sol et al. analyzed retrospectively by two radiologists. We investigated the data on patients with infectious complications within 30 days after stent placement. The data were assessed retrospectively by review of medical charts and imaging findings. In this study, early infectious complications consisted of acute cholangitis, acute, and liver abscess. Acute cholangitis was based on the presence of clinical symptoms such as body temperature greater than 38 C, leukocytosis, and chills in the absence of another explanation or on ultrasound and CT findings. Acute and liver abscess were diagnosed on the basis of the clinical symptoms, including leukocytosis, chills, and right upper quadrant pain with Murphy s sign, especially in cases of acute, and correlative CT or ultrasound findings. Stent Placement One experienced interventional radiologist performed all of the percutaneous transhepatic biliary drainage (PTBD) and stent placement procedures. All PTBD procedures were performed under sonographic and fluoroscopic guidance by a left ventral (n = 95) or right lateral (n = 99) approach or both approaches (n = 21) before stent placement. An 8- or 10-French soft silicon rubber drainage catheter (Dawson-Mueller, Cook) was used for the PTBD procedures. Among the 215 patients, 83 patients (38.6%) had undergone one or more failed endoscopic treatments before PTBD and stent placement. Most of the patients were given broad-spectrum IV antibiotics at least 48 hours before and after the procedure because they had the infectious symptoms, such as fever, chills, and leukocytosis, associated with biliary obstruction. All stents were percutaneously inserted through the PTBD track. If the segment obstructed by the tumor was short or there was no combined infection, both PTBD and stent placement were performed at the same time (one-stage procedure). If combined infection was present, PTBD was performed 2 or 3 days before stent insertion (twostage procedure). In patients with common bile duct obstruction, to identify and measure the length of unaffected distal common bile duct, percutaneous cholangiography was performed through the catheter during stent placement with the tip of the catheter positioned both immediately proximal and immediately distal to the stricture. Metallic stents were placed across the main duodenal papilla (transpapillary placement) when tumor obstructed the lower 2 cm of the common bile duct. When tumor spared and did not obstruct the lower 2 cm of the common bile duct, a stent was placed above the main duodenal papilla (nontranspapillary placement). A covered stent was used in patients with aggressive tumors such as pancreatic cancer and gallbladder cancer, and an uncovered stent was placed in patients with less aggressive tumors, such as a cholangiocarcinoma. To check stent function 3 7 days after insertion, the tip of the PTBD tube was placed immediately proximal to the stent. The PTBD tubes were removed in 3 7 days after stent placement, when follow-up cholangiography showed good passage of contrast medium through the stent and the serum total bilirubin concentration had decreased more than 30%. Statistical Analysis Statistical differences in sex, level of obstruction, type and number of stents, and stent position (across or above the main duodenal papilla) between patients with and those without early infectious complications were analyzed with the chisquare and Fisher s exact tests. The Student s t test was used to test differences between the two patient groups according to age. Stepwise logistic regression analysis was used for multivariate analysis. Values of p < 0.05 were considered statistically significant. All statistical analyses were performed with statistical software (SPSS 10.0, SPSS). Results All stents were percutaneously inserted through the PTBD track without technical difficulty. Four patients underwent stent insertion and PTBD in a one-stage procedure; the other 211 patients underwent PTBD 2 or 3 days before stent insertion (two-stage procedure). No procedure-related deaths occurred. Three patients (1.4%) had procedure-related complications such as mild transient hemobilia. A total of 120 patients underwent single stent placement, and 95 patients underwent T- or Y-configured dual stent placement. Uncovered stents were placed in 177 patients, and covered stents were placed in 38 patients. In 73 patients, stents were placed across the main duodenal papilla (transpapillary placement), and in 142 patients stents were placed above the main duodenal papilla (nontranspapillary placement). No deaths occurred within 30 days after stent placement, and no patients were lost to follow-up in this period. In this study, early (within 30 days) infectious complications after stent placement occurred in 14 of the 215 patients (6.5%) (six men, eight women; mean age, 67.8 years; range, 34 86 years). The patients without early infectious complications (114 men, 87 women) had a mean age of 66.9 years (range, 37 87 years). No significant differences between groups were found in age (p = 0.835, Student s t test) or sex (p = 0.313, chi-square test) (Table 1). Among the 215 patients, a hilar stricture was present in 121 patients and a distal biliary stricture in 94 patients. Causes of biliary obstruction were Klatskin tumor (n = 65), pancreatic cancer (n = 44), extrahepatic cholangiocarcinoma (n = 42), gallbladder cancer (n = 31), metastasis (n = 23), duodenal cancer (n = 2), cancer of the ampulla of Vater (n = 5), malignant intraductal papillary mucinous tumor (n = 2), and hepatocellular carcinoma (n = 1) (Table 2). Among 65 patients with Klatskin tumor, three patients had type 1, 14 patients had type 2, 23 patients had type 3A, five patients had type 3B, and 20 patients had type 4 tumors according to the Bismuth classification. There was no significant difference between patients with and those without complications with respect to level of malignant biliary obstruction (p = 0.082, chi-square test) (Table 1). Among the 14 patients with early infectious complications, acute cholangitis occurred in six patients, acute in 10 patients, and liver abscess in three patients. Three patients (patients 1, 3, 4) had both acute cholangitis and, and two patients (patients 2 and 10) had both acute and liver abscess. The characteristics of patients with early infectious complications are shown in Table 3. All 10 patients underwent percutaneous cholecystostomy immediately after the diagnosis of. The clinical outcome among the patients who underwent percutaneous cholecystostomy was good, all 10 patients recovering. Patients with acute cholangitis were treated with antibiotics. Patients with liver abscesses were treated with percutaneous drainage and antibiotics. All 14 patients with early infectious complications had undergone nontranspapillary stent placement. Among the patients without early infectious complications, 73 patients had undergone transpapillary stent placement and 128 patients had undergone nontranspapillary stent placement. As shown in Table 1, only stent placement above the main duodenal papilla was associated with the development of early infectious complications (p = 0.003, Fisher s exact test). Multiple logistic regression analysis showed no significant difference between the two groups in age, level of obstruction, and type and number of stents (Table 4). We inevitably excluded stent position as a factor because the 262 AJR:194, January 2010

Stent Insertion in Biliary Obstruction TABLE 1: Characteristics of Patients With and Without Early Infectious Complications Age (y) Characteristic Complication Present (n = 14) Mean 67.8 66.9 Range 34 86 37 87 Sex Men 6 114 Women 8 87 Level of obstruction Hilar stricture 11 110 Distal biliary stricture 3 91 Type and number of stent Single and covered stent 1 36 Single and uncovered stent 5 78 Dual (Y- or T-configured) stent 8 87 number of patients with transpapillary stent placement in the group with complications was zero, which was insufficient for satisfactory multiple logistic regression analysis. Discussion In this study, early infectious complications after stent placement occurred in 14 of 215 patients (6.5%). A 6.5 22% frequency of cholangitis after biliary stent placement has been reported in previous studies [10, 11, 20 22], and has been reported in as many as 1.9 12% of cases [14, 23]. Complication Absent (n = 201) p 0.835 a 0.313 a 0.082 a 0.476 a Stent position 0.003 Transpapillary 0 73 Nontranspapillary 14 128 a Not significant. The incidence of liver abscess after biliary stent placement has been reported to be 0.3 0.5% [10, 24]. Although the rate of early infectious complications in our study is close to the range in previous reports, our rate can be considered low because we included not only cholangitis but also and liver abscess. We believe the main reasons for this lower rate are as follows: First, a single experienced interventional radiologist performed all PTBD procedures and biliary stent placements, overcoming technical challenges. Second, PTBD tubes were removed TABLE 2: Causes of Malignant Biliary Obstruction Managed With Percutaneous Biliary Stent (n = 215) Diagnosis Hilar Stricture Distal Biliary Stricture Total Klatskin tumor 65 0 65 Pancreatic cancer 0 44 44 Extrahepatic cholangiocarcinoma 19 23 42 Gallbladder cancer 26 5 31 Metastasis 10 13 23 Duodenal cancer 0 2 2 Cancer of ampulla of Vater 0 5 5 Malignant intraductal papillary mucinous tumor 0 2 2 Hepatocellular carcinoma 1 0 1 Total 121 94 215 Note Values are numbers of patients. when stents exhibited good function and the serum total bilirubin concentration had decreased more than 30%. A self-expandable stent takes a few days to expand spontaneously, and it takes time for infectious symptoms and laboratory abnormalities to subside. Therefore, we usually removed the drainage tubes 3 7 days after stent placement. In our experience, successful stent placement combined with subsequent cholangiography to identify good stent function followed by removal of the PTBD tubes seems to be a good way to prevent early infectious complications. Third, broad-spectrum antibiotics were administrated before and after the procedure. Fourth, to our knowledge, in most other studies of cholangitis after biliary stent placement, stent placement was performed not only percutaneously but also endoscopically [13, 15 19, 23]. In this study, among the 14 patients with early infectious complications, acute occurred in 10 patients and required immediate percutaneous cholecystostomy. Although we did not investigate whether coverage of the cystic ducts by the stent induced acute, various reports have appeared. Miyayama et al. [25] reported that covering the cystic duct should be avoided to prevent. Inal et al. [7] reported that was caused by cystic duct obstruction by the stent. There is still controversy, however, about whether covering the cystic ducts with a stent is likely to induce acute. Only a small number of studies have been performed to compare the development of postprocedural cholangitis in patients with transpapillary stent placement with that in patients with nontranspapillary stent placement. Shimizu et al. [12] suggested that placing a stent across the main duodenal papilla might increase the incidence of cholangitis. Okamoto et al. [13] described 108 patients with malignant biliary obstruction treated with metallic stents. Cholangitis developed in 12 of the treated patients after stent placement. Eight patients had undergone transpapillary stent placement, and four patients had undergone nontranspapillary stent placement. The investigators concluded that placement of a biliary metallic stent across the main duodenal papilla may predispose patients to cholangitis. The results of the study by Okamoto et al. suggest that disruption of the sphincter mechanism by placement of a stent across the main duodenal papilla may be the most important etiologic factor in the development of cholangitis af- AJR:194, January 2010 263

Sol et al. TABLE 3: Characteristics of Patients With Early Infectious Complications After Percutaneous Biliary Stenting Patient No. Sex/Age (y) Diagnosis Complication 1 M/67 Klatskin tumor Cholangitis, 2 F/78 Extrahepatic cholangiocarcinoma Cholecystitis, liver abscess 3 M/53 Klatskin tumor Cholangitis, 4 M/66 Intrahepatic peripheral cholangiocarcinoma 5 F/80 Cancer of pancreatic head Cholangitis, Type and Number of Stent ter metallic stent placement for malignant biliary obstruction. The results of these previous studies differed from those of our study. Hatzidakis et al. [11] evaluated the use of metallic stents in the sphincter of Oddi for malignant obstructive jaundice when the tumor is more than 2 cm from the main duodenal papilla. Stents were placed above the papilla in 30 cases, and in another 30 cases they were placed with the distal part protruding into the duodenum. The difference in incidence of cholangitis in favor of patients in whom stents were placed above the papilla was statistically significant (p < 0.05). The investigators concluded that for patients with extrahepatic lesions more than 2 cm from the papilla, the sphincter of Oddi also should be stented to reduce postprocedural morbidity. In our study, all 14 patients with early infectious complications had undergone nontranspapillary stent placement, and univariate analysis showed a statistically significant difference (p = 0.003, Fisher s exact test). Our result was similar to that of Hatzidakis et al. The exact etiologic factor in the development of cholangitis is unknown. It has been hypothesized to be preservation of sphincter function and inherently poorer biliary drainage. Huibregtse et al. [19] suggested that insertion of a stent across the main duodenal papilla might be preferable to preservation of function of the main duodenal papilla because of better bile drainage across the sphincter. In this study, there was no significant difference between the two groups regarding type of stent, that is, covered or uncovered. Among the 120 patients who underwent single stent placement, early infectious complications occurred in one of 37 patients (2.7%) with covered stents and five of 83 patients (6.0%) with uncovered stents. However, there was no statistically significant difference with respect to stent type (p = 0.665, Fisher s exact test). TABLE 4: Results of Multiple Logistic Regression According to results of many previous studies, whether a covered or uncovered stent is likely to induce acute cholangitis remains controversial. Park et al. [17] examined the use of both covered (n = 98) and uncovered (n = 108) stents (Wallstent, Boston Scientific) in patients with malignant extrahepatic biliary obstruction to determine whether use of covered stents prolonged stent patency without increasing the rate of procedure-related complications. Acute occurred in five of 88 patients who received covered stents and one of 100 patients who received uncovered stents. Although patients who received covered stents appeared to Variable Odds Ratio 95% CI p Sex 1.81 0.60 5.50 0.30 Age 1.01 0.95 1.06 0.94 Level of obstruction 0.34 0.07 1.66 0.18 Number and type of stent Stent Location Time Between Procedure and Identification of Infection (d) Management of Acute Cholecystitis Single, covered 1.00 0.82 Single, uncovered 1.98 0.21 18.65 0.55 Dual, Y- or T-configured 1.57 0.15 16.94 0.71 Duration of Cholecystostomy Tube Insertion (d) Uncovered, dual Nontranspapillary 23 Cholecystostomy 4 Uncovered, single Nontranspapillary 8 Cholecystostomy 3 Uncovered, dual Nontranspapillary 2 Cholecystostomy 3 Uncovered, single Nontranspapillary 9 Cholecystostomy 9 Cholecystitis Uncovered, single Nontranspapillary 8 Cholecystostomy 2 6 F/62 Klatskin tumor Cholecystitis Uncovered, dual Nontranspapillary 7 Cholecystostomy 3 7 M/81 Klatskin tumor Liver abscess Covered, dual Nontranspapillary 21 8 F/80 Klatskin tumor Cholecystitis Uncovered, single Nontranspapillary 7 Cholecystostomy 2 9 F/51 Klatskin tumor Cholangitis Uncovered, dual Nontranspapillary 28 10 F/77 Gallbladder cancer Cholecystitis, liver abscess Covered, single Nontranspapillary 2 Cholecystostomy 9 11 F/86 Klatskin tumor Cholecystitis Uncovered, single Nontranspapillary 3 Cholecystostomy 7 12 F/34 Metastasis Cholecystitis Uncovered, dual Nontranspapillary 4 Cholecystostomy 14 13 M/78 Metastasis Cholangitis Uncovered, dual Nontranspapillary 5 14 M/56 Metastasis Cholangitis Uncovered, dual Nontranspapillary 8 264 AJR:194, January 2010

Stent Insertion in Biliary Obstruction have a higher incidence of acute than patients who received uncovered stents, the difference was not statistically significant (p = 0.104). Isayama et al. [18] reported the results of a prospective randomized study on the use of covered (n = 57) and uncovered (n = 55) diamond stents in the management of distal malignant biliary obstruction. The incidence of covered stent occlusion was significantly lower than that of occlusion of uncovered stents. The cumulative patency of covered stents was significantly higher than that of uncovered stents. However, acute occurred in two of 42 patients (4.8%) in the final covered-stent group and in none of the uncovered-stent group. Mild pancreatitis occurred in five patients (8.7%) in the covered-stent group and in no patient in the uncovered-stent group. The investigators therefore recommended that careful attention be paid to complications specific to the use of covered self-expandable metal stents, such as acute and pancreatitis. Our study had limitations. First, the data were collected retrospectively, so selection bias occurred because only patients who underwent percutaneous biliary stent insertion were included. Second, not every patient underwent regular follow-up imaging examinations and laboratory testing. Third, the relatively small number of patients with early infectious complications may have been another limitation; therefore, the numerical difference between the groups with and without complications is quite large. Fourth, as described earlier, we could not use stent position as a factor in multivariate analysis because of inevitable statistical problems. However, univariate analysis sufficiently showed that the presence of early infectious complications had a positive association with transpapillary stent placement. 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