Percutaneous Metallic Stents in Patients with Obstructive Jaundice due to Hepatocellular Carcinoma

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1 Percutaneous Metallic Stents in Patients with Obstructive Jaundice due to Hepatocellular Carcinoma Hyun Pyo Hong, MD, Seung Kwon Kim, MD, and Tae-Seok Seo, MD PURPOSE: To evaluate the technical success and clinical efficacy of percutaneously placed self-expandable metallic stents in patients with obstructive jaundice due to hepatocellular carcinoma (HCC). MATERIALS AND METHODS: Fifteen men (mean age, 59.3 years) with obstructive jaundice resulting from HCC were treated with self-expandable metallic stents (28 stents in 19 sessions). The authors evaluated the technical success, clinical success (decrease of 30% of total serum bilirubin level <2 or mg/dl [34.2 mol/l]), treatment efficacy according to lowest total serum bilirubin level, complications, and duration of stent patency. RESULTS: Technical success was achieved in all patients. Clinical success was achieved in 11 of the 15 patients (73% After stent placement, seven patients (47%) had a low bilirubin level <2 mg/dl ( [34.2 mol/l]), three (20%) had an intermediate bilirubin level (2 10 mg/dl [ mol/l]), and five (33%) had a high bilirubin level >10 ( mg/dl [171 mol/l]). A low bilirubin level was achieved in all patients with Child-Pugh A disease and stage T2 or T3 HCC. Maj complications such as hemobilia necessitating transfusion n ( 1) or abscess formation n ( 1) occurred in two of the 19 sessions (10%). The overall mean stent patency was days (range, days). The mean stent patency i patients with Child-Pugh class A disease (257.8 days) was significantly longer than that of patients with Child-Pugh class B and C disease (123.2 and 63 days, respectively) P <.05). ( CONCLUSIONS: The percutaneous placement of a self-expandable metallic stent is a feasible and effective palliative treatment for patients with obstructive jaundice resulting from HCC, especially for those with Child-Pugh class A disease and stage T2 or T3 HCC. J Vasc Interv Radiol 2008; 19: Abbreviations: HCC hepatocellular carcinoma, PTBD percutaneous transhepatic biliary drainage, TACE transcatheter arterial chemoembolization IN patients with hepatocellular carcinoma or progression of an underlying cir-to a cholangiocarcinoma, pancreatic (HCC), jaundice usually manirhosis (1,2). In a small proportion ofcarcinoma, gallbladder carcinoma, fests at a late period of illness andpatients with HCC, the bile duct canand metastatic lymphadenopathy 10 ( represents a poor prognosis. Jaundice be obstructed by extrinsic compres- 13). Because obstructive jaundice is by the HCC, direct invasion of the uncommon in patients with HCC and is usually due to tumor destruction ofsion the liver parenchyma, hilar invasion, HCC, or metastatic lymph nodes 3 ( most patients have a bleeding ten- due to cirrhosis, a percutane- 8). The relief of the biliary obstructiondency can be a good palliative treatment andously placed self-expandable metallic From the Department of Radiology, Kangbuk Samsung can improve the quality of life andstent is not widely used in the treatment Hospital, Sungkyunkwan University School of of obstructive jaundice resulting survival of the patient. Lau et al 9) ( Medicine, 108, Pyung-Dong, Jongro-ku, Seoul, Korea (H.P.H., S.K.K.); and the Department of reported that the overall survival offrom HCC. Radiology, Guro Hospital, Korea University College patients with HCC and obstructive We hypothesized that percutane- placement of a self-expandable of Medicine, Seoul, Korea (T.S.S.). Received August jaundice who were treated by meansous 7, 2007; final revision received December 30, 2007; of curative resection, biliary stents, metallic stent could be a good palliative treatment in patients with ob- accepted December 31, Address correspondence to S.K.K.; radi@lycos.co.kr and supportive treatment appeared to have been improved. structive jaundice from HCC and that None of the authors have identified a conflict of interest. The use of a self-expandable metal-ilic stent is a well-established methodcatheter arterial chemoembolization would be possible to continue trans- SIR, 2008 DOI: /j.jvir for palliating a patient with an inoper-(taceable malignant biliary obstruction due system. Herein, we wanted to after decompression of biliary analyze 748

2 Volume 19 Number 5 Hong et al 749 the technical success, clinical efficacy, and limitation of percutaneously placed self-expandable metallic stents in patients with obstructive jaundice from HCC according to different Child-Pugh classes, the T stage of HCC, and the type of hilar obstruction. Therefore, the purpose of this study was to report our experience on the use of palliative treatment for patients with obstructive jaundice resulting from HCC and to evaluate the technical success and clinical efficacy of the percutaneously placed self-expandable metallic stents. MATERIALS AND METHODS Study Patients The institutional review boards of two hospitals approved this retrospective study, and all patients signed statements giving their informed consent. From December 2004 to February 2006, we retrospectively reviewed the medical records and the images of 15 patients with obstructive jaundice due to HCC who were treated with selfexpandable metallic stents in two hospitals. All patients were men, and their mean age was 59.3 years (range, years). Four patients had Child-Pugh class A disease, seven had class B disease, and four had class C disease. Eleven patients had undergone TACE for HCC days (mean, 57 days) before stent placement, whereas four patients were admitted with obstructive jaundice and were then diagnosed as having HCC. TACE was performed via the microcatheter with transarterial infusion of a mixture of iodized oil (Lipiodol; Andre Guerbet, Aulnaysous-Bois, France) and doxorubicin hydrochloride (Adriamycin; Dong-A Pharm, Seoul, Korea), and doses depended on the size and vascularity of the tumor. The diagnosis of HCC was made on the basis of characteristic computed tomographic (CT) findings and elevation of the -fetoprotein level ( 400 ng/ml [ g/l]). Biopsy was not performed to confirm the diagnosis of HCC. A diagnosis of HCC as the cause of obstructive jaundice was made with CT findings such as tumor compression of the intrahepatic or extrahepatic bile duct or dilatation of the bile duct with an intraductal tumor. The mean HCC diameter at contrast medium enhanced CT was 9 cm (range, 4 16 cm). HCC was classified as nodular (n 6), massive (n 8), or diffuse (n 1) according to the Eggel classification (14). Three patients had stage T2 HCC, one patient had stage T2 HCC, and 11 patients had stage T4 HCC. The types of hilar obstruction were assessed with CT and cholangiographic findings according to the Bismuth classification and were evaluated by two radiologists (H.P.H., S.K.K.) in consensus. A Bismuth type I lesion involves the main hepatic duct more than 2 cm from the hilum, and a type II lesion involves the hilum with obstruction of both the right and left hepatic ducts. A type III lesion involves the segmental biliary ducts in one lobe, and a type IV lesion involves the extension of the tumor to the segmental ducts in both lobes (15). Five patients had type II hilar obstruction, five had type III obstruction, and five had type IV obstruction. Techniques All percutaneous transhepatic biliary drainage (PTBD) procedures were performed with use of ultrasonographic (US) and fluoroscopic guidance by means of a left ventral approach (n 2), right lateral approach (n 9), or both (n 4) (16). Broadspectrum antibiotics (cefazolin, 1 g intravenously) were given for 12 hours before and after each procedure. Procedures were performed with the patient under local anesthesia with 2% lidocaine HCl (Myung Moon Pharmaceutical, Hwaseong, Gyeonggi, Korea) and intravenous conscious sedation with 50 mg pethidine HCl (Hana Pharmaceutical, Hwaseong, Gyeonggi, Korea). Balloon dilation of the stenosis before stent placement (predilation) was not performed. Twenty-eight stents were placed in 19 sessions. Single-duct drainage was achieved in seven patients with the placement of one stent. In eight patients, two stents were placed through dual PTBD tracts (Y configuration) (n 4) or a single PTBD tract (T configuration) (n 4) to maintain two-duct drainage. During follow-up, stent occlusion by tumor ingrowth or overgrowth occurred in two patients, so three additional sessions with four stents were performed in one patient (Fig 1) and one additional session with one stent was performed in another patient. We used various kinds of self-expanding nitinol stents in this study. The following stents were used: Hanaro stent (MI Tech, Seoul, Korea) (n 17), transverse stent with a T configuration (Kim stent; Taewoong, Seoul, Korea) (n 2), transverse stent with a T configuration (MI Tech) (n 1), Hercules stent (S & G Biotec, Seoul, Korea) (n 4), Zilver stent (Cook, Bloomington, Indiana) (n 2), and Sentinol stent (Boston Scientific, Natick, Massachusetts) (n 2). In four patients, eight stents were placed in the hepatic hilum with a Y configuration by using separate stents. In another four patients, eight stents were placed in a T configuration by using Kim stents (n 2) or a Hanaro stent (n 1) with a large mesh or a conventional mesh through technique (n 1). For the conventional mesh through technique, the secondary stent was placed through the mesh of a primary stent followed by dilation with a 10-mm angioplasty balloon. The mean time between PTBD and stent placement was 20.5 days (range, days). In 12 of the 15 patients, stents were placed within 13 days after the initial drainage procedure, and in the remaining three patients, stents were placed days after the initial drainage procedure. One to 7 days after stent placement, a cholangiogram was obtained to confirm the position and patency of the stents, and the external drainage catheters were removed in 10 sessions for eight patients. Although the patency of the stents was confirmed with cholangiography, drainage catheters were kept in the remaining seven patients due to a high bilirubin level. Follow-up The patients were followed at monthly intervals during the follow-up period. Medical records were reviewed, US or CT of the liver was performed, and serum bilirubin levels were checked. Technical success was defined as placement of a stent providing continuous drainage of bile. Clinical success was defined as a decrease in the serum bilirubin level of more than 30% relative to the baseline value or a serum bilirubin level of less

3 750 Biliary Stents in Patients with Hepatocellular Carcinoma May 2008 JVIR ; SPSS, Chicago, Illinois). Treatment efficacy according to the lowest poststent total serum bilirubin level was analyzed according to different Child-Pugh classes, the T stage of HCC, and the type of hilar obstruction with use of the Fisher exact test. Mean stent patency rates were analyzed for different Child classes, the T stage of HCC, and the type of hilar obstruction with use of the Kruskal-Wallis test. If the results of analysis of variance were statistically significant, comparisons were applied with the Mann-Whitney U test. Stent patency rates were plotted with the Kaplan-Meier method. A Cox proportional hazards model was used to assess differences affected by the Child-Pugh class, T stage of HCC, or type of hilar obstruction. RESULTS Figure 1. Patient 2. Images in a 63-year-old man with obstructive jaundice resulting from a HCC. (a) Axial contrast-enhanced CT scan obtained before stent placement shows partial iodized oil uptake by the HCC (arrows) in the severe atrophic right lobe of the liver and dilation of both intrahepatic ducts (arrowheads). The HCC compresses the confluence of both intrahepatic ducts. The total bilirubin level was 9.6 mg/dl (164 mol/l). (b) Cholangiogram obtained 3 days after stent placement demonstrates full expansion of the stent (arrows) and good bile passage. There was no significant bleeding during PTBD and stent placement. After normalization of the bilirubin level, an additional TACE procedure was performed. (c) Stent occlusion by tumor overgrowth occurred, and an additional stent was placed. Cholangiogram obtained 3 days after the second stent placement demonstrates the expansion of the second stent (arrows) and good bile passage. During the follow-up period, stent occlusion by tumor overgrowth recurred, and an additional two sessions of stent placement were performed. than 2 mg/dl (34.2 mol/l) within 30 days after stent placement. We classified treatment efficacy as low bilirubin level ( 2 mg/dl [34.2 mol/l]), intermediate bilirubin level (2 10 mg/dl [ mol/l]), and high bilirubin level ( 10 mg/dl [171 mol/l]) according to the lowest poststent total serum bilirubin level because efficacy of biliary stents could not be evaluated in patients with underlying severe hepatic insufficiency or extensive parenchymal destruction by HCC and total serum bilirubin level must be less than 2 mg/dl (34.2 mol/l) to be eligible for TACE. Complications of the procedure were classified as major or minor according to the reporting standards of the Society of Interventional Radiology (17). Stent patency was defined as the period between insertion and stent occlusion (increase in bilirubin level). In cases of recurrent jaundice or an increase in bilirubin level, patients were evaluated with US, percutaneous transhepatic cholangiography, or CT. At the time of death, a stent was considered to be patent if the patient had a normal bilirubin level or no increase in the total bilirubin level. Statistical Analysis Statistical analysis was performed with use of a software package (SPSS The clinical and stent data for the 15 patients are summarized in Table 1. Stent placement was technically successful in all patients. Improvement of the itching sensation was achieved in 14 of the 15 patients (93%), and improvement of general jaundice symptoms (eg, yellow skin and icteric sclera) disappeared in seven (47%) patients. Clinical success was achieved in 11 of the 15 patients (73%). Fourteen of the 15 patients had a statistically significant decrease in the serum bilirubin level 30 days after stent placement (mean standard deviation, 15.5 mg/dl 2.82 [265 mol/l 48] before the procedure and 6.7 mg/dl 1.91 [114 mol/l 33] after the procedure). A paired t test comparing pre- and postprocedural mean bilirubin levels showed a P value of less than.05, which was considered to be statistically significant. In one patient with Child-Pugh class C disease, the total bilirubin level continuously increased even after stent placement. This might be due to combined liver parenchymal destruction by the tumor and hepatic insufficiency. Treatment efficacy for the 15 patients according to the Child-Pugh stage, T stage of HCC, and type of hilar obstruction are summarized in Tables 2 4. A low bilirubin level 2( mg/dl [34.2 mol/l]) was achieved in seven patients (47%), an intermedi-

4 Volume 19 Number 5 Hong et al 751 Table 1 Summary of Clinical and Stent Data Patient No./ Age (y) jor complications such as hemobilia necessitating transfusion (n 1) or abscess formation (n 1) occurred in two sessions (10%) (Fig 2). An additional transcatheter arterial embolization was not needed for hemobilia. Hepatic abscess was successfully treated with percutaneous catheter drainage, and the catheter was eventually removed. The mean stent patency time was days (range, days). There was a statistically significant difference in stent patency among Child- Pugh class A, B, and C disease (Kruskal-Wallis test, P.05). The mean stent patency in patients with Child-Pugh class A disease (mean, days) was significantly longer than that of patients with class B (mean, days) and C (mean 63 days) disease (P.05, Mann-Whitney U test). There was no statistically significant difference in stent patency with regard to T stage and obstruction type (P.05). According to Cox proportional hazards analysis, the stent patency rates were affected by the Child-Pugh class (P.05). The stent patency rates were not affected by the T stage and ob- Child- Pugh Class Tumor Size (cm) T Stage Obstruction Type* Time between PTBD and Stent Placement Stent Configuration Stent Length (cm)/ No. of Stents No. of Sessions Total Bilirubin Level Before Stent Placement (mg/dl) After Stent Placement (mg/dl) Following Treatment 1/72 C 8 4 III 13 Single 9/ NA 2/63 A IV 6 Single 7,8,10/ TACE 3/62 B III 5 Single 7/ NA 4/66 B 9 4 III 7 T 6,10/ NA 5/68 B 11 4 IV 3 Single 9,10/ TACE 6/81 C IV 7 Y 8,10/ NA 7/36 B III 11 Single 9/ NA 8/54 B II 4 Single 10/ NA 9/41 C III 8 T 8/ NA 10/1 B II 5 Y 8,10/ NA 11/53 C II 7 T 6,10/ NA 12/59 A 6 2 IV 140 T 6,9/ NA 13/56 A 3 2 II 95 Single 8/ TACE 14/50 A 4 4 II 7 Y 7,8/ TACE 15/58 B 4 2 IV 58 Y 5,8/ NA * Determined with the Bismuth classification. Single one stent was placed through a single puncture site, Y two stents were placed through two separate puncture sites, T two stents were placed through the same puncture site. NA not available. The total bilirubin levels in these patients before stent placement were less than 2 mg/dl because they had long-term percutaneous drainage tubes before stent placement. Table 2 Lowest Poststent Total Serum Bilirubin Level according to Child-Pugh Class Child-Pugh Class Low ( 2 mg/dl) ate bilirubin level (2 10 mg/dl [ mol/l]) was achieved in three patients (20%), and a high bilirubin level ( 10 mg/dl [171 mol/l]) was seen in five patients (33%). The low bilirubin rate (100%) of patients with Child-Pugh class A disease was significantly higher than that (27%) of patients with Child-Pugh class B and C disease (P.05). The low bilirubin rate (100%) of patients with stage T2 and T3 HCC was significantly higher than that (27%) of patients with stage T4 HCC (P.05). A low bilirubin level was achieved in three of the five patients with type II obstruction, none of the five patients Lowest Total Serum Bilirubin Level Intermediate (2 10 mg/dl) High ( 10 mg/dl) A(n 4) B(n 7) C(n 4) Total with type III obstruction, and four of the five patients with type IV obstruction. The difference in the number of patients with low bilirubin levels according to type of obstruction was not statistically significant (P.05). After improvement of the patient condition, an additional TACE procedure was performed in four patients. No procedure-related deaths occurred. Overall, complications occurred in seven of the 19 sessions (37%). Minor complications such as bile leakage (n 4) and self-limiting hemobilia (n 1) occurred in five sessions (26%). Bile leakage was treated with dressing or catheter change. Ma-

5 752 Biliary Stents in Patients with Hepatocellular Carcinoma May 2008 JVIR Table 3 Lowest Poststent Total Serum Bilirubin Level according to T Stage T Stage struction type. The patency curves according to the Child-Pugh class are shown in Figure 3. DISCUSSION Low ( 2 mg/dl) Several studies describe the percutaneous placement of self-expandable metallic stents for malignant biliary obstruction including HCC. The number of patients with HCC in these studies, however, is small, and HCC was not evaluated independently (12,13,18,19). To our knowledge, this study is the largest study of percutaneous self-expandable metallic stent placement for the treatment of obstructive jaundice resulting from HCC. Lau et al (9) studied 49 patients with HCC and obstructive jaundice. Among the 49 patients, 27 were treated with an endoscopic stent, five were treated with a percutaneous stent, nine received curative resection, and five had supportive treatment to relieve the obstructive jaundice. The overall survival of these 49 patients was similar to that of patients who presented with no clinically detectable jaundice and was much better than Lowest Total Serum Bilirubin Level Intermediate (2 10 mg/dl) High ( 10 mg/dl) T2 (n 3) T3 (n 1) T4 (n 11) Total Table 4 Lowest Poststent Total Serum Bilirubin Level according to Obstruction Type Obstruction Type Low ( 2 mg/dl) Lowest Total Serum Bilirubin Level Intermediate (2 10 mg/dl) High ( 10 mg/dl) II (n 5) III (n 5) IV (n 5) Total Note. Obstruction type was classified with the Bismuth classification. that of patients with jaundice due to hepatic insufficiency. These investigators concluded that, with proper management like curative resection or endoscopic and/or percutaneous stents, good palliative and occasional cure were possible in patients with HCC with obstructive jaundice. Clinical success was achieved in 11 of our 15 patients (73%) with obstructive jaundice resulting from HCC treated with self-expandable metallic stents. This clinical success rate is slightly lower than that with percutaneous placement of self-expandable metallic stents for other malignant biliary obstructions (12,13,18,19). However, we achieved clinical success in all patients with Child-Pugh class A disease and staget2 or T3 HCC. We also analyzed the stent patency and treatment efficacy according to the obstruction type. Overall, the mean stent patency in our study was days. This stent patency was comparable to that reported in previous studies that were focused on malignant hilar obstruction, including a cholangiocarcinoma, gallbladder carcinoma, and metastatic lymph node at the hilum (16,18). Because there were no statistically significant difference with regard to low bilirubin level and duration of stent patency according to obstruction type (P.05), the type of biliary obstruction appeared not to correlate with the low bilirubin rate and duration of stent patency. Although the prognosis of a patient with HCC and an obstructive jaundice is better than that of a patient with a similar HCC and a jaundice due to hepatic insufficiency, the prognosis of a patient with HCC and obstructive jaundice is generally poor (9,20,21). A percutaneously placed self-expandable metallic stent is not widely used for the treatment of obstructive jaundice due to HCC. HCC is a highly vascular tumor, and most patients have a bleeding tendency due to cirrhosis. A subsequent hemorrhage and hemobilia could be serious complications after PTBD and stent placement. Hemorrhage and hemobilia may cause stent obstruction, transfusion, arterial embolization, and additional stent placement and may increase patient morbidity and mortality. In our study, self-limiting hemobilia (n 1) and hemobilia necessitating transfusion (n 1) occurred in two sessions (10%). An additional transcatheter arterial embolization was not needed for hemobilia. There was one hepatic abscess formation, and it was successfully treated with percutaneous catheter drainage. This complication rate is similar to that for biliary stent placements with other malignant tumors (12,13,18,19). Therefore, the percutaneous placement of self-expandable metallic stents is a feasible and safe treatment for patients with obstructive jaundice resulting from HCC. The purpose of placing a self-expandable metallic stent is not only to improve jaundice and pruritus, but also to give the opportunity for further palliative treatment such as TACE. A bilirubin level of more than 1.5 mg/dl (26 mol/l) is known to be predictive of decreased patient survival (22). Many systemic chemotherapy regimens require intact mechanisms of bilirubin excretion and bile drainage for efficacy and to prevent toxicity (23). Although endoscopic biliary drainage is one of the most effective treatments for patients with unresectable malignant biliary stenosis, it is often difficult to perform in the patient with HCC and may fail because of proximal biliary obstruction at the hilum and an

6 Volume 19 Number 5 Hong et al 753 Figure 2. Patient 10. Images in a 71-year-old man with obstructive jaundice resulting from a HCC. (a) Axial contrast-enhanced CT scan obtained before stent placement shows a diffuse HCC with left portal vein thrombosis (arrows) and mild dilation of both intrahepatic bile ducts (arrowheads). The total bilirubin level was 10 mg/dl (171 mol/ L). (b) Cholangiogram obtained 6 days after two stents were placed through dual PTBD tracts (Y configuration) demonstrates full expansion of the stents (arrows) and good bile passage. The total bilirubin level was normalized after stent placement. (c) Axial contrastenhanced CT scan obtained after 1 month shows a 3.4-cm abscess cavity (arrows) in segment VII of the liver. (d) The abscess cavity was treated with use of 8.5-F percutaneous catheter drainage (arrows). Figure 3. Graph shows stent patency according to Child-Pugh class. Data were determined with Kaplan-Meier analysis. The mean stent patency in patients with Child-Pugh class A disease (mean, days) was significantly longer than that in patients with class B (mean, days) and C (mean, 63 days) disease (P.05, Mann-Whitney U test). underlying cirrhosis (24). Although major complications were more common in the percutaneous placement of self-expanding metal stents than in endoscopic retrograde cholangiopancreatography stent placement (25), endoscopic retrograde cholangiopancreatography stent placement is also an invasive procedure with major potential for procedure-related complications such as pancreatitis, hemorrhage, perforation, cholangitis, and cardiorespiratory compromise (26). Four of the 15 patients (27%) who had a significant decrease in the bilirubin level after metallic stent placement were eligible for further TACE on the basis of this response. After improvement of the patient condition, an additional TACE procedure was performed in four patients. Therefore, biliary stent placement in patients with HCC can relieve jaundice, ensure a better quality of life, allow for a further TACE procedure, and, possibly, prolong survival (7,26,27). The stent patency rates were affected by the Child-Pugh class (P.05, Cox proportional hazards analysis). The Child-Pugh class was a better predictor of stent patency than was the T stage and obstruction type. Therefore, the decision to place the self-expandable metallic stent in patients with obstructive jaundice caused by HCC should primarily be based on the extent of hepatic functional reserve. There are several limitations to this study. First, this is not a prospective, randomized study and, therefore, we cannot conclude with absolute certainty that there is a possible benefit to the use of self-expandable metallic stents in patients with obstructive jaundice resulting from HCC. Second, the sample size may not provide enough power to identify differences among the subgroups and prognostic factors other than the Child-Pugh class. In conclusion, percutaneous placement of self-expandable metallic stents is a feasible and effective palliative treatment in patients with obstructive jaundice resulting from HCC, especially for those with Child- Pugh class A disease and stage T2 or T3 HCC. However, there is limited clinical efficacy for patients with Child-Pugh class B and C disease or stage T4 HCC.

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