Prognostic effects of different malignant obstructive jaundice sites on percutaneous biliary intervention: A retrospective controlled study : Journal of Cancer Research and Therapeutics

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Original Article

Prognostic effects of different malignant obstructive jaundice sites on percutaneous biliary intervention: A retrospective controlled study

Xu, Junming; Zhuang, Shaowu; Liu, Mingqiang; Wu, Songhui; Li, Huajie

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Journal of Cancer Research and Therapeutics 19(1):p 78-85, March 2023. | DOI: 10.4103/jcrt.jcrt_2038_22
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Abstract

INTRODUCTION

Malignant obstructive jaundice (MOJ) is the narrowing or occlusion of the normal anatomy of the bile duct caused by the invasion and compression of malignant tumors, such as bile duct cancer, hepatocellular carcinoma, pancreatic cancer, gallbladder cancer, and metastatic cancer, in or around the bile duct.[1] The main objective of treating MOJ is to reduce jaundice, and percutaneous perforated hepatic biliary drainage or combined stent placement is the treatment regimen for patients with inoperable MOJ.[2]

Several studies have confirmed that percutaneous transhepatic cholangial drainage (PTCD) is an effective treatment for jaundice,[3] and percutaneous transhepatic biliary stenting (PTBS) is also an effective long-term treatment for obstructive jaundice. Xu et al.[4] demonstrated that stenting had a significantly longer median survival than biliary drainage (243 days vs. 161 days); the long-term prognosis of PTBS was relatively better than that of biliary drain,[5] and the reduction in bilirubin levels was approximately the same for both.[4]

There have been studies that have reported and analyzed the factors influencing PTCD or PTBS for patients with MOJ in terms of survival,[6,7] including patient survival quality score, liver function Child-Pugh score, types of tumor, duration of obstruction, and postoperative infection.[8,9] Owing to the multiplicity of malignant tumors causing MOJ and the special anatomical structure of the bile ducts, tumor-derived stenosis or obstruction may occur from the extrahepatic common bile duct sphincter of Oddi, the plane of the bile cyst duct to the second and third branches of the right and left intrahepatic bile ducts,[10] and different levels of obstruction will affect the efficacy and survival of MOJ treatment. At present, only a few studies have mentioned the possible prognostic impact of different biliary obstruction levels,[8,11,12] and no specific grading has been described. In this study, we aimed to investigate and analyze the factors associated with survival after MOJ treatment by retrospectively examining the differences in survival and complications after transbiliary stenting combined with biliary drainage treatment at different sites.

SUBJECTS AND METHODS

Patients

This was a retrospective comparative study, and patient data collection was approved by the Ethics Committee of our Hospital. A total of 120 patients with MOJ treated with PTBS combined with biliary drainage in our hospital from January 2017 to December 2021 were included, and all patients underwent imaging examinations, such as ultrasound, CT, or MRCP, to clarify the extent of bile duct dilatation and the site of obstruction. The biliary obstruction planes were classified according to biliary anatomy as obstruction from the confluence of the right and left bile ducts to the common hepatic duct (high-position group, n = 36), from the opening of the cystic duct to the opening of the pancreatic duct in the common bile duct segment (middle-position group, n = 43), and in the hepatopancreatic ampulla segment of the common bile duct (low-position group, n = 41, including 3 patients with both middle and low position of MOJ). Among them, only 18 patients had a clear pathological diagnosis of MOJ. The cases without a pathological diagnosis were evaluated by the multidisciplinary team, including interventional radiology, gastroenterology, medical oncology, and hepatobiliary procedure, in terms of their clinical symptoms, relevant laboratory tests and imaging testing for features, the clinical diagnosis of MOJ, and the indications for interventional treatment; the therapies were selected according to the degree of obstruction and the mode of obstruction. While some patients with large obstructions, bile duct occlusion, rapid tumor progression, and high restenosis rate were evaluated and treated with a combination of intraluminal brachytherapy.[13]

Inclusion and exclusion criteria were as follows: inclusion criteria: age 18–80 years; pathologically confirmed or clinically diagnosed MOJ; no indication for radical surgical treatment; physical status ECOG score 0–3; exclusion criteria: extensive systemic tumor metastasis; treatment by PTCD alone; and incomplete follow-up data. We initially included 153 patients with MOJ. Based on the inclusion and exclusion criteria, 120 patients were included in this study [Figure 1].

F1
Figure 1:
Flow chart of the study on different parts of patients with malignant obstructive jaundice

Materials and device

Biliary self-expanding smart metal stent (8–10-mm diameter, Cordis Medical, Ciudad Juarez, Mexico), percutaneous puncture introducer kit (TERUMO, Beijing, China), PTA balloon dilation catheter (Boston Scientific, Cork, Ireland), drainage catheter kit (ARGON MEDICAL, Athens, TX), digital subtraction angiography system (DSA, Philips Professional Healthcare, Eindhoven, Netherlands), and portable ultrasound equipment (GE Volusion, Marlborough, US).

The 125I radioactive 125I particles (4.5 mm in length, 0.8 mm in diameter, and an activity of 0.6–0.8 mCi, High-Tech Atom, Beijing, China) were configured in a cylindrical brachytherapy source encapsulated by titanium. The number of 125I seeds to be implanted was calculated as N = stent length (mm)/4.5 + 4,[14] and the particles were encapsulated in 4 F sterile clear tubing inside the drainage kit. The ends of these ports were closed by heated with high temperature.

Interventional treatment procedure

Prophylactic antibiotics were used before, during, and 1 day after interventional procedures, and analgesics (fentanyl or meperidine) were permitted. Under ultrasound and DSA guidance, the bile duct branches were dilated intrahepatically via percutaneous puncture using an 18G needle, a guide wire was introduced, and a 6F vascular sheath was introduced in exchange. If the stenosis is low in the bile duct and the edge of the stenosis is >1 cm from the sphincter of Oddis, the stent should be placed without damaging the sphincter of Oddis as much as possible. In the left or right intrahepatic bile ducts, usually 6 mm diameter stents were chosen, but in the common bile duct (CBD), the diameter of the stent used depended on the maximum diameter of the CBD. If the CBD diameter was <10 mm, 8-mm or 10-mm diameter stents were usually used bilaterally. After successful stent placement, an external drain or internal and external drain was placed through the guide wire. For patients undergoing stenting combined with intraluminal brachytherapy, the vascular sheath was inserted and two guide wires were introduced through the vascular sheath. With one of the guide wires being introduced into the long vascular sheath first, the stent was placed along the other guide wire, and a custom 125I particle chain was pushed in along the long sheath for placement, with the particle chain being secured between the stent and bile duct wall [Figure 2].

F2
Figure 2:
(a-c) 54-year-old male with hilar cholangiocarcinoma and obstructive jaundice. Intraoperative Cholangiography suggested interrupted continuity and filling defects in the right and left intrahepatic bile ducts (white arrows) (high obstruction); Parallel biliary stents (left 8 mm × 60 mm, right 8 mm × 80 mm) combined with 125I particle chain (16 chains) were implanted via bilateral access and treated with external drainage to relieve the obstruction. (d-e) 54-year-old male with recurrent postoperative lymph node metastasis in the hilar region and obstructive jaundice after gastric cancer. Cholangiogram after 1 month of percutaneous transhepatic cholangial drainage revealed a common bile duct below the cystic duct (medium obstruction). A biliary stent (8 mm × 80 mm) combined with 125I particle chain (15 chains) was inserted via the right side access, and the balloon (6 mm × 80 mm) was posteriorly dilated, preserving the sphincter of Oddis and achieving intra-stent patency. (f-g) 60-year-old male with pancreatic head cancer and obstructive jaundice. Cholangiography showed occlusion of the jugular segment of the common bile duct (low obstruction). A biliary stent (10 mm × 60 mm) combined with 125I particle chain (10 chains) was placed via the right side access and drained externally, and the sphincter of Oddis could not be retained

The drainage tube was clamped 48 h postoperatively and removed after 2–4 weeks. After interventional therapy, further antitumor therapy was given according to the primary disease and general condition of the patient, which mainly included systemic chemotherapy, primary trans-arterial chemoembolization, arterial perfusion chemotherapy, image-guided local ablation, 125I particle implantation therapy, targeted drugs, and immune checkpoint inhibitor therapy.

Follow-up

The follow-up period began from the postoperative period, where follow-up visits were conducted at the 1st, 2nd, and 3rd months, and then at 3-month intervals until the patient died or reached the end of the clinical study if the disease was stable. Laboratory tests and imaging were performed at postoperative months 1, 2, 3, 6, 12, 18, and 24. The follow-up period ended on December 31, 2021. The endpoint of this study was survival. The differences in 1-year survival, stent patency, pre- and post-procedure bilirubin and liver function changes, and complications were studied. Survival was defined as the time interval between stent implantation and death from any cause or the last follow-up visit. Stent patency was defined as the time interval between stent implantation and stent occlusion or the time to last follow-up or death for those who did not experience restenosis.

Statistical analysis

The statistical software SPSS Statistics 26.0 (Armonk, NY: IBM Corp) was used for statistical analysis. The basic information of different biliary obstruction site groupings was compared by the descriptive analysis method. Categorical variables were described by n (%), and comparisons were made using Pearson’s Chi-square analysis. Continuous variables were first tested using ANOVA or non-parametric tests for normality, described by for linearity and median (P25, P75) for nonlinearity. For between-group confounding factors, Cox regression models were chosen to control baseline unstable variables.

The Kaplan–Meier curve was used to test the survival of each group and to compare the difference in survival among the three groups. The paired-sample t test or Kruskal–Wallis test was used to compare liver function status and stent patency time before and after treatment within each group. The effect of subgroups and other risk factors on 1-year survival was analyzed using multifactorial Cox regression. P < 0.05 was considered a statistically significant difference.

RESULTS

Patient groups

Table 1 summarizes the clinical baseline characteristics of the three groups of patients. There were no significant differences between the three groups in terms of sex, age, total bilirubin (TBIL), alanine transaminase (ALT), aspartate transaminase (AST), preoperative PTCD, intraluminal brachytherapy, and postoperative antitumor therapy. Because of the different types of malignant tumors causing obstruction, the features of biliary obstruction at different horizontal levels, and the limited sample size of each group in a single centre, there was an imbalance between groups in terms of two indicators, direct bilirubin (DBIL), and serum creatinine (SCR) (P < 0.05). Considering the small sample size within each group, it was not appropriate to apply a propensity score (PSM) to these unbalanced variables. For the subsequent between-group comparison study, we pre-emptively applied a multifactorial Cox regression model to control the abovementioned four unbalanced variables in order to weaken or eliminate the effects of these confounding factors.

T1
Table 1:
Clinic characteristics of 120 patients with patients with malignant obstructive jaundice

Survival

In terms of the observation endpoint, the Kaplan–Meier curve [Figure 3] showed that the high-position group had a longer survival than the other two groups, with a median overall survival (OS) of 16 months in the high-position group (95% CI: 11.8, 20.2), 8.6 months in the middle-position group (95% CI: 4.4, 12.8), and 5.6 months in the low-position group (95% CI: 3.9, 7.3). There was a statistically significant difference in OS between the high- and low-position groups (P = 0.017), while the difference between the middle-position group and the other two groups was not statistically significant (vs. high-position group, P = 0.336, vs. low-position group, P = 0.358) [Figure 3].

F3
Figure 3:
Overall survival rate of three groups after percutaneous transhepatic biliary stenting

Effect of different obstruction sites on the 1-year survival rate of MOJ

The 1-year survival rate was 67.6% in the high-position group, 41.9% in the middle-position group, and 41.5% in the low-position group (P < 0.05), and the survival advantage at 1 year was more pronounced and statistically significant in the high-position group compared to that in the other two groups (vs. middle-position group P = 0.024, vs. low-position group P = 0.05) [Figure 4]. We used multifactorial Cox regression to analyze the effect of different stent placement sites on 1-year survival, and the results showed that after adjusting for potential confounding factors, the 1-year risk of death was 2.35 (95% CI: 1.12–4.91) and 2.93 (95% CI: 1.38–6.21) times higher in the middle- and low-position groups, respectively, than in the high-position group, using the high-position group as a control [Table 2].

F4
Figure 4:
Overall survival of three groups in 1 year
T2
Table 2:
Effect of different obstruction sites on the 1-year survival rate of malignant obstructive jaundice

Complications

Complications were assessed according to the Common Terminology Criteria for Adverse Events (CTCAE 5.0). The incidence of grade 3 or 4 complications—major postoperative complications (including operation-related biliary tract infection, hemorrhage, thoracoabdominal effusion, and renal failure) was 25% (9/36), 48.8% (21/43), and 65.9% (27/41) in the high-, middle-, and low-position groups, respectively, with statistically significant differences among the three groups (P = 0.002). The complications with the highest probability in each group were mainly biliary tract infections. Severe biliary tract infections combined with sepsis and infectious shock were mainly observed in the low-position group (5/41, 12.2%); two cases of postoperative abdominal hemorrhage occurred, both in the middle-position group (4.7%), which improved after hemostatic treatment; one case of acute pancreatitis occurred in the middle-position group after procedure, which was cured after anti-infection, pancreatic secretion suppression, and symptomatic treatment.

There were 12 cases of internal and external drainage applications in our center. The incidence of biliary tract infection was 75%, while the incidence of infection in external drainage (108 cases) was 16.1% (high-position group), 34.3% (middle-position group), and 58.8% (low-position group). In addition, 14 patients opted for elective PTBS after PTCD, with an infection rate of 28.6%.

The grade 1 or 2 complications (Minor complications) mainly included postoperative abdominal pain, vomiting, hypothermia, and self-limiting hemorrhage, and the incidence of minor complications was 19.4% in the high-position group, 39.5% in the middle-position group, and 58.5% in the low-position group (58.5%), with statistical differences between groups (P = 0.002). Postoperative abdominal pain was the common in all groups, and it was mostly relieved by symptomatic treatment. No stent or 125I particle chain displacement or breakage was observed in all patients. [Table 3]

T3
Table 3:
Complications after percutaneous transhepatic biliary stenting at different obstruction sites, n (%)

Comparison of stent patency after PTBS at different obstruction sites

The median stent patency in each group was 8.95 months in the high-position group, 4.6 months in the middle-position group, and 4.3 months in the low-position group, with no statistically significant difference between the three groups (P > 0.05) [Table 4].

T4
Table 4:
Comparison of stent patency after percutaneous transhepatic biliary stenting at different obstruction sites

Comparison of liver function indicators before and after surgery at different obstruction sites

The liver function indicators ALT, AST, and TBIL levels were significantly reduced in all three groups at 1-month and 3-month postoperative follow-up, except for the middle-position group, where the ALT level was approximately the same as before at 3 months postoperatively, and the other two groups showed a continuous reduction (P < 0.05). A similar trend was observed for AST levels (P < 0.05). In addition, there was a trend of sustained reduction of the TBIL level at 1 month and 3 months postoperatively in all groups (P < 0.001). However, there was no significant difference in the decrease in ALT, AST, or TBIL levels between the groups at 1 month and 3 months postoperatively (P > 0.05). [Supplementary Tables S1-3]

T5
Supplementary Table S1:
Comparison of alanine transaminase status before and after surgery at different stent placement sites
T6
Supplementary Table S2:
Comparison of pre- and postoperative aspartate transaminase status at different stent placement sites
T7
Supplementary Table S3:
Comparison of pre- and postoperative total bilirubin status at different stent placement sites

DISCUSSION

MOJ can occur at any level within the bile duct because of the diversity of the malignant tumor causing the obstruction and the site of metastasis, most commonly in the hilar and distal bile ducts.[15,16] Only a few studies in the literature have mentioned high and low obstruction (high obstruction is defined as being above the junction of the bile cyst duct and common hepatic duct; and low obstruction is defined as being below the junction of the bile cyst duct and common hepatic duct) and essentially only focused on the treatment study of a certain obstruction level, such as malignant obstruction in the hilar region[16] or biliopancreatic pot belly.[17] The effect of different bile duct obstruction sites on patient survival after MOJ stenting has not been reported in the literature. Therefore, we attempted to perform a group study with different levels of bile duct obstruction.

In terms of the criteria for grouping, we investigated and considered the actual clinical situation.[10] Using bile duct cancer as an example, the latest anatomical classification includes the proximal end of the secondary branches of the bile duct, the opening of the cystic duct, and the hepatopancreatic ampulla as the boundary.[18] In terms of our discussion of MOJ, the classification of cholangiocarcinoma does not apply to this study because of the distinction between different tumor obstruction sites. For example, some patients require double-stent placement or left and right bile duct drainage for obstructive jaundice caused by Bismuth III and IV types of hilar cholangiocarcinoma, and the risk of increased adverse effects remains controversial.[19] For MOJ in the hepatopancreatic ampulla, stent placement may affect the function of the sphincter of Oddis, thus increasing the incidence of postoperative complications, especially biliary tract infections,[12,20] which was also confirmed by the comparison of complications in this study [Table 3]. Therefore, different outcomes may occur with bile duct stenting at different levels of bile duct obstruction, and a controlled study was conducted based on the left and right bile duct confluence areas, the opening of the cystic duct, and the hepatopancreatic ampulla, which were divided into high-, middle-, and low-position groups according to the location of obstruction. However, we collected 3 cases of MOJ happened both in middle- and low-position, 2 cases of pancreatic head cancer and 1 case of cholangiocarcinoma, because of the more aggressive invasiveness of malignant tumors. These cases were implanted longer metal stents combined with intraluminal brachytherapy and the Oddis sphincters were not retained, which was consistent with the treatment method and prognosis characteristics of low-level MOJ, as a consequence, these cases were classified into the low-position group.

After controlling for patient baseline confounding factors (especially tumor type) using Cox multifactorial regression, this study found that MOJ in the hilar region, compared to MOJ in the middle and lower bile ducts, could achieve relatively long OS and a relatively low risk of death at 1 year after PTBS. We believe that this result corresponds to its complication rate, which was the lowest in the high-position group. Intervention-related biliary tract infections are one of the most common complications following biliary obstruction treatment.[20] Because treatment requires percutaneous puncture, the rich vascularity along the puncture path may cause an increased risk of sepsis, while severe infection is a leading cause of death in patients.[21] The choice of drainage method is also important. Xu et al.[22] compared internal and external drainage and infection after external drainage for MOJ. The results showed that the infection rate of internal and external drainage was significantly higher than that of external drainage alone. Another study confirmed that the mortality rate after internal and external drainage was significantly higher than that after external drainage or biliary stent placement.[23–25] According to the results of this study, the risk of infection from internal and external drainage is relatively higher than that of external drainage. The risk of infection by external drainage was relatively low in the high- and middle-position groups, but it remained high in the low-position group, with most of the cultured bacteria coming from the gut, which was thought to be related to retrograde infection of the gut microbiota as a result of Oddis sphincter disruption. In addition, for patients with severe preoperative biliary tract infection, PTCD followed by elective PTBS was associated with a lower infection rate (28.6%), although whether this reduces the risk of infection needs to be confirmed in a large sample size.

In this study, the serum TBIL, ALT, and AST levels of the three groups at 1 month and 3 months after biliary implantation were significantly lower than those before interventional therapy, with no significant difference in the magnitude of reduction, indicating that biliary stent placement can effectively achieve biliary drainage and improve liver function regardless of the level of obstruction. In terms of stent patency, although the median patency was significantly longer in the high-position group than in other groups, the Kruskal–Wallis non-parametric test showed no statistical difference (non-normal distribution had more pronounced skewness). Considering the small sample size, large intra-group differences, and possible influence of survival, the results still need to be supported by a larger sample size.

This study has limitations. First, the current study is a retrospective cohort study involving a relatively small population in a single institutional center, and the quality of the study sample cannot be effectively controlled. It is inevitable to have confounding factors, which need to be eliminated by applying statistical techniques in order to eliminate the influence of confounding factors. Therefore, we are conducting a multicenter, prospective, randomized, and controlled study. Second, selection biases might be existing in terms of the type of tumor, which is determined by the characteristics of MOJ in different parts, however, it did not meaningfully affect the choice of treatment modality. Finally, radiation might affect other people in close contact with the patients, but prudent precautions have been taken to reduce the contact with others.

In conclusion, the different levels of biliary obstruction in patients with MOJ impact the survival, especially the 1-year survival rate, of biliary stenting. The obstruction in the hilar region has a relatively smaller incidence of complications and a lower risk of death after treatment compared to the obstruction in the hepatopancreatic ampulla, and the appropriate treatment for different biliary sites may be beneficial to patient prognosis. For different levels of biliary obstruction, biliary stent placement is effective in achieving biliary drainage and improving liver function.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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Keywords:

Malignant obstructive jaundice; overall survival; percutaneous biliary intervention; prognostic effects; sites

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