Intraoperative Effects of Preoperative Biliary Metallic and Plastic Stents in Malignant Pancreatic Head Tumors: Surgeon Perspective

The ethical approval for this study was taken from the Avrasya Hospital ethical committee with the number 2016-75. Between December 2016 and January 2018, patients who had preoperative endoscopic biliary drainage and were operated consequently were divided into 2 groups: group 1 (n = 29): metallic stent group, and group 2 (n = 101): plastic stent group.

Our inclusion criteria were operable pancreatic head carcinoma. If the patients had signs of infection, they were excluded. The surgery of all patients was elective and the levels of C-reactive protein, leukocytes, and procalcitonin were recorded preoperatively. Antibiotics were not routinely used but all patients were treated with preoperative antibiotic prophylaxis. Patients were operated because their bilirubin levels reduced under 4 mg/dL. All patients were operated by the same surgical team. Pylorus-preserving pancreaticoduodenectomy was the standard surgical procedure for all patients. Intraoperative surgical difficulty was evaluated by an independent surgeon and classified via visual analog scale from 1 to 10. Biliary stents were removed and sent to culture intraoperatively. Two drains were placed in all patients. In case of suspicion about infection in the field of surgery, cultures were taken for aerobic, anaerobic, and fungal organisms. Patients with severe pancreatic fistula in the postoperative period and the patients with infection in the preoperative period were excluded from this study. Wound and surgical site infections, fistula rates, and hospital stay were compared between the 2 groups.

In the postoperative period, the infection findings were determined by clinical fever, positive microbiological culture, and imaging methods. Bacteremia-positive blood culture was determined by taking 2 consecutive blood samples in patients with fever of 38 degrees C.

Quantitative data are presented as mean ± SD. Data transformation by square root was applied to the operative time and stent type during surgery to meet the normality requirement. Operative time and stent type were standardized by minusing their mean and dividing by their SD. Student t test or χ² test was applied to examine the difference of each variable as indicated. Linear regression was used to determine the relationships between the patients’ variables and endpoints (operative time and stent type), whereas logistic regression was applied for postoperative morbidity. After univariate analysis, variables with a P < 0.25 were selected for multivariate analysis. A multivariate analysis was performed using multiple linear regression or logistical model, with a stepwise (forward selection/backward elimination) method. The statical analysis was performed using SPSS 16.0 (SPSS Inc., Chicago, Illinois). Differences were considered statically significant if the P value was equal to or less than 0.05 with a 95% confidence interval.

A total of 130 (80 male and 50 female) patients were evaluated. In group 1, there were 20 male and 9 female patients. In group 2, there were 82 male and 19 female patients. Mean age in group 1 was 57.9 ± 13.4, and 63.8 ± 9.0 in group 2. There was no statistically significant difference between the 2 groups in terms of mean age, operation time, intraoperative bleeding, hospital stay, and surgical difficulty (respectively P = 0.34, P = 0.25, P = 0.52, P = 0.96, P = 0.41). Demographic data of the patients are shown in Table 1.

Univariate analysis showed that body mass index (P = 0.0005) was the only factor associated with surgical difficulties. Our results also showed that operative time was not significantly associated with stent type.

Thirteen of 29 patients (44.8%) had positive biliary stent cultures in group 1, whereas 80 of 101 (79%) patients had positive biliary stent cultures in group 2. The positive culture rate was statistically higher in the plastic stent group, and the negative culture rate was statistically higher in the metallic stent group (respectively, P = 0.001 and P < 0.05). Relation between stent types and intraoperative stent culture results are shown in Table 2.

Postoperative fistula rates were 17.2% in the metallic stent group and 9.9% in the plastic stent group. Relation between stent types and postoperative pancreatic fistula rates are shown in Table 3.

In our study, there was no observed direct complication related to stents. When stent cultures were examined for microorganisms, it was detected that Streptococcus anginosus had more growth in both groups. When postoperative wound infection was compared, the level of wound infection in group 2 was higher than in group 1 but its relation to stents is not fully understood. Intraoperative bile culture and microorganisms and infectious complications are shown in Tables 4 and 5.

Preoperative stenting and infectious complications based on stents in cholestatic icterus patients have been frequently studied in the literature. However, it has not been investigated whether these infectious complications are related to the type of stents (metallic or plastic). In general, metallic stenting is used for patients who are locally advanced or cannot be operated. This is because of the idea that metallic stents make the operations more difficult and increase intra-abdominal adhesion independent of the operations.

Pancreatic head tumors are commonly presented with jaundice clinically. Prolonged jaundice may cause various nutritional disorders, impaired wound healing, and increased postoperative complications in patients.^8–10  Because of such negative effects, preoperative biliary drainage is performed for patients who have high bilirubin levels or cholangitis.^11,12  The literature showed that the risks of infectious complications, intra-abdominal abscess, and death were increased with biliary drainage. In another multicenter randomized trial, it was shown that preoperative biliary drainage resulted in a 2-fold increased rate of serious complications compared with the patients who underwent surgery alone. However, no significant differences were found in surgery-associated complications, length of hospital stay, or mortality.^12,13  Although no comparison was made with patients who did not receive stents in our study, no significant difference was found in terms of surgical difficulty between patients who received different types of stents.

Endoscopic interventions are usually preferred in biliary drainage and stents are commonly used for this purpose.^14–16  Preoperative biliary stenting was introduced in 1970. There is no consensus on bilirubin levels and application methods of endoscopic drainage interventions in the literature.^17,18  Theoretically, no beneficial effect of preoperative biliary stenting could be demonstrated yet. In high-volume centers, less traumatic and more effective methods to decrease bilirubin levels are preferred according to the clinical condition of the patient.^19,20  We also usually prefer endoscopic methods for biliary stenting in our clinic. Biliary stent types may vary according to operability of the patient. Plastic stents are usually preferred in operable patients, whereas metallic stents are preferred in borderline or inoperable patients. Plastic stents and metallic stents provide similar short-term results with respect to clinical success, morbidity, mortality, and improvement in quality of life. Among plastic biliary stents, polyethylene models allow relief of obstruction more frequently than Teflon-made stents of the Tannenbaum or Amsterdam type; among currently available self-expanding metallic stent models, no significant differences were reported at 30 days (Evidence level 1 + +). Patient-related factors associated with failure to resolve jaundice after biliary stenting include a high baseline bilirubin level, diffuse liver metastases, and International Normalized Ratio ≥1.5 (Evidence level 2 +). After biliary stenting, the patient is taken for surgery following recovery of vital signs and sufficient decrease in bilirubin levels.²¹  On the other hand, patients with pancreatic adenocarcinoma usually present with locally advanced, unrespectable, or metastatic disease.¹²  In this group of patients, biliary decompression may be required for palliation. Montero et al¹³  presented the results of their study regarding the cost-effectiveness of metallic stents in pancreatic cancer. The study included patients with locally advanced pancreatic cancer who underwent endoscopic retrograde cholangiopancreatography with metallic or plastic stent placement. The results suggest that patients with metallic stents had lower costs and greater overall and quality-adjusted survival. Specifically, the investigators found that metallic stent implementation resulted in approximately $1500 saved per patient over a lifetime and fewer stents placed (mean number: 1.4 versus 2.8). Moreover, metallic stenting improved overall survival by 0.07 months and the quality-adjusted survival by 0.10 months.

Endoscopic stenting disturbs attending surgeons because of its intraoperative effects on inflammation and intensive adhesions that may cause surgical difficulty in dissection and increased postoperative complications.^22–24  We wait 4 to 6 weeks after biliary stenting for effective bilirubin decrease and recovery of the patient from cholangitis to avoid intraoperative difficulties. Despite prolonged waiting time, relatively difficult dissection is inevitable in endoscopic stent patients. The most valuable result of our study is high positive culture rates, especially in plastic stent patients (80%). However, high positivity in stent cultures does not cause increased surgical site infections. In addition, stent type does not affect operation time, hospital stay, surgical difficulty, postoperative pancreatic fistula, and surgical site infection rates. In a retrospective analysis, it was reported that preoperative stenting did not have a negative effect on surgical difficulty but increased postoperative infectious complications.⁵  A recent prospective study compared 2 groups of patients, one had preoperative biliary stenting and the other did not, and reported that postoperative complications were higher in the biliary stent group. Review of the surveillance, epidemiology, and end results (SEER) database of 1992–2007 indicated that the trend of preoperative biliary stent use of surgeons has not changed.

To the best of our knowledge, this is the first study in the English literature that evaluates the effect of preoperative stent types on postoperative complications. According to our study, preoperative metallic stent use has an advantage on effective bilirubin decrease until surgery and has lower positive stent culture rates. However, there was no clinical reflection of the difference in stent culture positivity between the 2 groups. In contrast to the common belief that metallic stents cause surgical difficulties, our study reports no statistically significant increase in surgical difficulty due to metallic stent use.

Preoperative biliary stent use of surgeons has not altered recently according to the literature. The possible reason may be that gastroenterologists are usually the first who see the patient and they took endoscopic retrograde cholangiopancreatography and stenting before surgery in their algorithm. Despite the delay to the surgery, preoperative covered metallic stents provide effective bilirubin decrease with lower obstruction rates and intraoperative stent culture positivity. High bilirubin levels are not a contraindication for surgery as a common opinion. However, in case of preoperative endoscopic biliary drainage, use of metallic stents is more advantageous than plastic stents.

The authors would like thank Dr. Serap Durmuş for help with the manuscript, data correction, and results. Author contributions: Ali Durmuş: Conceptualization, data curation, formal analysis, funding acquisition, methodology, project administration. Oguzhan Karatepe: Supervision, validation, visualization. data curation, formal analysis. Ugur Kesici: Software, writing – original draft, writing – review & editing, investigation, resources. The authors have no conflict of interest or financial support. The data that support the findings of this study are available from the corresponding author on reasonable request. No additional data are available. This study was conducted between December 1, 2016, and January 30, 2018, with approval from the Private Avrasya Hospital Ethics Committee (approval date/no: 02.01.2016/75). The study was conducted in accordance with the Declaration of Helsinki. Patients were not required to give informed consent to the study because the analysis used anonymous clinical data that were obtained after each patient agreed to treatment by written consent.