Journal of Gastrointestinal Surgery

, Volume 15, Issue 3, pp 489–495

Radical Surgery in the Presence of Biliary Metallic Stents: Revising the Palliative Scenario

Authors

  • Dimitrios Lytras
    • Department of SurgeryUniversity College of London Hospitals NHS Foundation Trust
  • Steven W. M. Olde Damink
    • Department of SurgeryUniversity College of London Hospitals NHS Foundation Trust
  • Zahir Amin
    • Department of RadiologyUniversity College of London Hospitals NHS Foundation Trust
  • Charles J. Imber
    • Department of SurgeryUniversity College of London Hospitals NHS Foundation Trust
    • Department of SurgeryUniversity College of London Hospitals NHS Foundation Trust
Original Article

DOI: 10.1007/s11605-010-1389-2

Cite this article as:
Lytras, D., Olde Damink, S.W.M., Amin, Z. et al. J Gastrointest Surg (2011) 15: 489. doi:10.1007/s11605-010-1389-2
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Abstract

Background

The application of endobiliary self-expandable metallic stents (SEMS) is considered the palliative treatment of choice in patients with biliary obstruction in the setting of inoperable malignancies. In the presence of SEMS, however, radical surgery is the only curative option when the resectability status is revised in case of malignancies or for overcoming complications arising from their application in benign conditions that masquerade as inoperable tumours. The aim of our study was to report our surgical experience with patients who underwent an operation due to revision of the initial palliative approach, whilst they had already been treated with biliary SEMS exceeding the hilar bifurcation.

Methods

Three patients with hilar cholangiocarcinoma that was considered inoperable and one patient with IgG4 autoimmune cholangio-pancreatopathy mimicking pancreatic cancer underwent radical resections in the presence of biliary SEMS.

Results

After a detailed preoperative workup, two right trisectionectomies, one left extended hepatectomy and a radical extrahepatic biliary resection were performed. All cases demanded resection and reconstruction of the portal vein. R0 resection was achieved in all the malignant cases. Two patients required multiple biliodigestive anastomoses entailing three and seven bile ducts respectively. There was one perioperative death due to postoperative portal vein and hepatic artery thrombosis, whilst two patients developed grade III complications. At follow-up, one patient died at 13 months due to disease recurrence, whilst the remaining two are free of disease or symptoms at 21 and 12 months, respectively.

Conclusions

Revising the initial palliative approach and operating in the setting of biliary metallic stents is extremely demanding and carries significant mortality and morbidity. Radical resection is the only option for offering cure in such complex cases, and this should only be attempted in advanced hepatopancreaticobiliary centres with active involvement in liver transplantation.

Keywords

Self-expanding metallic stentsCholangiocarcinomaBile ductHilar tumoursHepatic confluence

Introduction

The application of self-expanding metallic stents (SEMS) as palliative treatment of inoperable biliary and pancreatic malignancies is currently a widely established and accepted practice.1 SEMS offer improved patency and significantly lower rates of obstruction compared with the plastic stents, and they are considered as the palliative method of choice for patients with a life expectancy of more than 6 months.2,3 However, the disadvantage of occlusion due to in-growth or overgrowth phenomena does exist, whilst their rapid incorporation into the bile duct wall due to the foreign body reaction makes them almost irremovable.4 So far, the only indication for embarking in a surgical attempt in the setting of metallic stents' presence is either the revision of a “non-resectable” diagnosis for malignant entities, or the necessity for relieving the complications of the SEMS when they xare placed in benign cases mimicking inoperable neoplasms.35 Scarce reports exist in the literature regarding the surgical experience and the challenges arising in the presence of biliary metallic stents. We report herein our experience in four patients within the last 2 years who were initially treated palliatively with uncovered SEMS as inoperable cases.

Materials and Methods

Between September 2007 and September 2009, 81patients with a diagnosis of inoperable cholangiocarcinoma (CCA) were assessed in the setting of our multidisciplinary hepatopancreaticobiliary (HPB) meetings for biliary malignancies. Seventeen patients were already treated by SEMS insertion elsewhere as inoperable hilar CCA, and they were referred for palliative treatment or potential enrolment in clinical trials. Diagnosis of inoperability was revised for three of these 17 patients following evaluation by our multidisciplinary team. The initial assessment precluding surgical resection was either extension of the tumour in second-order biliary radicles or portal vein involvement. Additionally, one more patient was referred due to multiple episodes of cholangitis in the presence of a SEMS inserted for palliation of metastatic pancreatic cancer with nodal involvement. However, final histology revealed IgG4 autoimmune cholangio-pancreatopathy (AICP).

Description of the Stents

In all cases, the proximal end of the SEMS was located above the biliary bifurcation. In two patients with cholangiocarcinoma, bilateral metallic stents were placed during the initial management. The third patient with CCA had a well-functioning solitary metallic stent draining the main right hepatic duct. The stent was placed after an exploratory laparotomy where the patient was judged as inoperable due to positive biopsies of the portal nodes. The fourth patient with autoimmune cholangio-pancreatopathy had a stent just passing the hepatic confluence proximally, but entering the duodenum distally (Table 1).
Table 1

Patient characteristics

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Description of Stents’ Side Effects

The duration from the time of stenting until the time of operation was 5 ± 8.5 months. Only one among these patients remained free of episodes of cholangitis after stent insertion, reaching the time of operation without any additional drainage intervention. The other three patients had all dysfunctioning stents which required endoscopic retrograde cholangiopancreatography (ERCP) for the removal of debris, ERCP twice plus percutaneous transhepatic drainage (PTD) and ERCP twice with placement of plastic stents through the metal ones plus PTD, respectively. The duration of primary stent patency was 45 and 92 days for the two patients with CCA who experienced cholangitis, whilst the first episode of stent obstruction in the patient with AICP developed at 213 days. Preoperative values of bilirubin were 67, 98, 12 and 16 μmol/L for the cases, respectively.

Preoperative Workup

All patients underwent a thorough preoperative evaluation with multi-detector contrast-enhanced computed tomography according to standardised liver and pancreatic protocols and/or magnetic resonance cholangiopancreatography. Repeat ERCP was performed in all cases for the assessment of pathology, definition of the proximal and distal stent level or as attempts to relieve jaundice prior to surgery. In order to achieve preoperative levels of bilirubin <50 μmol/L and treat segmental cholangitis as well, two patients required percutaneous transhepatic drainage.

Additionally, positron emission tomography was performed in two CCA patients for the exclusion of any distant metastatic deposits. Based on CT volumetry, one patient underwent portal vein embolization prior to the planned extended right hepatectomy for inducing hypertrophy of the future left liver remnant.

Laparoscopic assessment of the abdominal cavity for disease dissemination was performed in two patients with CCA and also in the patient with the presumed pancreatic cancer.

Results

All patients with diagnosis of hilar cholangiocarcinoma underwent extended liver resections. According to the Brisbane classification, there were two right trisectionectomies and one left extended hepatectomy (SgI + middle hepatic vein).6 The patient with AICP required extrahepatic bile duct resection and a high hilar hepaticojejunostomy entailing both the major ducts. All cases required portal vein resection and reconstruction either for securing negative resection margins, or due to technical demands arising from the dense fibrosis caused by the inflammatory response of the existing stent. However, no vein graft was used. Additionally, one patient (case 3) required resection and reconstruction of the right hepatic artery in combination with portal vein resection.

The stents were removed en bloc with the surgical specimen in two cases and in the remaining two, they had to be removed wire by wire due to extensive incorporation into the tissues. In the case of the patient with AICP, the distal part of the stent was cut at the level of the supra-pancreatic margin of the common bile duct (CBD) and remained in situ in order to avoid injury of the ampulla and the option of a pancreatoduodenectomy. The stump of the distal CBD was closed in a running fashion with Prolene 3/0. The number of the anastomosed bile ducts was one, three, seven and two, respectively. In all the cases of liver resections where multiple anastomoses were needed, every effort was made to approximate the exposed neighbouring subsegmental ducts into common channels for reducing the number of biliodigestive anastomoses. A fine-bore feeding catheter (4F) was used as stent of the anastomosis in two cases for minimising the risk of bile leak from high-risk reconstruction and this was externalised through the stump of the intestinal Roux-en-Y loop. The catheter was left in place for 35 and 42 days, respectively. Mean operative time was 8.58 h (range, 6.1–12 h), whilst the average operative blood loss was 2.7 U (range, 0–6 U). The number of frozen-section biopsies for the three malignant cases was three, five and nine, respectively. All the vascular resection margins were proven free of tumour invasion, and an R0 resection was achieved in all the malignant cases. Mean duration of hospital stay was 19 days (range, 9–27 days).

In histology, evidence of cholestasis was present in one case, whilst large duct obstruction and ascending cholangitis with abscess formation was prominent in the background liver of another patient (Fig. 1).
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Fig. 1

a, b Right trisectionectomy (case 1). a “Parenchyma first” approach and complete exposure of the left Glissonian pedicle at the level of SgII–SgIII bile duct bifurcation. Metal stent (white arrow) within the left hepatic duct. b Transection of the left hepatic duct above the proximal end of the metal stent. SgII–III bile duct (white arrow), umbilical branch of left portal vein (black arrow)

One patient with CCA died within the immediate postoperative period. He developed portal vein and hepatic artery thrombosis following a right trisectionectomy combined with portal vein and hepatic artery resection and reconstruction. Despite relaparotomy and embolectomy, he died on the ninth postoperative day due to multiple organ failure. There was only one patient with postoperative bile leak after liver resection, in combination with severe wound infection. He was treated with drainage of the collection under ultrasound guidance and long-term application of a vacuum-assisted closure pump. Additionally, the patient with AICP developed portal vein thrombosis and required long-term treatment with anticoagulants. In accordance with the classification for surgical complications of Dindo et al.,7 there were 25% grade IV, 50% grade III and 25% grade II complications, respectively.

In follow-up, one patient with CCA died at 13 months due to disease recurrence, whilst the third one remained free of disease at 21 months after the operation. The patient with AICP remains free of cholangitis episodes in 12 months of follow-up, with evidence of cavernous transformation of the porta hepatis.

Discussion

Endobiliary self-expanding metallic stents are considered the management of choice for palliation of inoperable biliary and pancreatic malignancies.19 However, in the setting of high volumes referral centres, the possibility of revising the initial diagnosis of irresectability or facing the complications of metallic stents inserted for benign conditions is indeed a reality and a challenging situation as well.

According to a systematic appraisal of the role of SEMS in the treatment of benign bile duct stricture, Siriwardana et al.3 reported the need for operative removal of occluded metallic stents in 9% among 400 cases due to complications not amenable to conservative endoscopic management. Additionally, Vibert et al.8 has reported in five cases with benign disease where SEMS were inserted in the setting of a diagnosis which was later revised at a tertiary HPB institute.

A detailed multimodal imaging evaluation is the first and most important great importance, step in the initial assessment of these patients. We consider the most useful combination to be of CT/MRI compounded with biliary imaging and particularly percutaneous transhepatic cholangiography. However, overcoming the difficulties in imaging interpretation due to artefacts caused by the presence of SEMS is mandatory in order to attempt a surgical intervention in this setting.10 Evaluating the proximal and distal extent of both the disease and the SEMS, as well as the potential vascular involvement in the radial axis as, is extremely challenging in the background of the inflammatory response caused by the SEMS. Lack of advanced imaging and interventional modalities, as well as HPB-focused radiologists and endoscopists in the referring institutes, might explain, in part, the primary palliative management of these cases. Referral biases may also influence the number of cases reaching a tertiary centre whilst still operable or before the development of complications due to the long-term presence of SEMS.

All our patients with a diagnosis of CCA were managed with extended liver resections in an effort to achieve both the mandatory clear margins from oncological perspective and to overcome the proximal level of the inserted stent as well. This necessity resulted in performing multiple biliodigestive anastomoses in two out of the three cases, entailing three and seven segmental ducts, respectively.

In all our cases, vascular resection and reconstruction was proven necessary since the dense fibrotic reaction at the porta hepatis and the hepatoduodenal ligament demanded meticulous sharp dissection of the stented biliary tree and radical resections of the adjacent portal vein. The combination of the desmoplastic reaction of the cholangiocarcinoma tumours and the inflammatory tissue response caused by SEMS, must be taken into account either for oncological reasons or due to the operative difficulties during the dissection of the common bile duct from major vascular structures. The rate of vascular resections in our series is significantly higher compared with that reported by Vibert et al. where only one among five cases demanded portal vein resection. The most likely explanation is the malignant nature of the pathology in most of our cases, in contrast with the benign entities faced by the previous group of authors. It could be speculated that, in our series, this fact resulted in higher vascular resection and reconstruction rates. In support of this, high rates of vascular resections up to 38%, have been reported by Mullen et al.11 in pancreatoduodenectomies for pancreatic malignancies that were stented with metallic stents prior to the operation. Although the duration of SEMS' presence and the progressive incorporation of the stents into the tissues could be another predisposing factor to this, it was, however, substantially shorter (5 months in our series) compared with the one reported in the study by Vibert et al.

We did not find necessary the use of interposition grafts for portal vein reconstruction in our cases. Indeed, when performing a right trisectionectomy, the mobilisation of SgIV portal branch and the extensive mobilisation of the portal vein (PV) trunk, in addition to the mobilisation of the umbilical portion of the left PV at the groove of Rex, allows a long segment (up to 5–7 cm) for primary reconstruction in most cases. In the left extended hepatectomy, we similarly dissected the right PV bifurcation of the first and even second order. This allows resections of PV segments of at least 4 cm.

The true dilemma on top of the possibility of dissecting the vessel is the one relating to oncological safety. The incomplete reliability of frozen sections, the difficulty in sampling and the differential diagnosis between fibrotic reaction secondary to SEMS and carcinoma are the challenges in these cases. This has prompted our aggressive policy of vascular resections, which yielded satisfactory results.

A technical aspect of major importance is the quality of bile duct mucosa at the resection margin and the safety of the structured anastomosis. Although the ideal approach would be to achieve a resection margin beyond the limit of the stent, this was not always feasible. Instead of extending the margins of the parenchyma resection, risking the loss of functional liver volume, we applied the alternative of transecting the stent below its proximal end and removing the metal mesh wire by wire from the anastomotic biliary stump. This manoeuvre offers the advantage of avoiding excessive mucosa detachment during the stent extraction. Additionally, the resulting, stent-free, extra bile duct length can be resected with safety at the level of less inflammatory mucosa, promoting the quality of the anastomotic tissues.

There was one postoperative death in our series due to hepatic artery and portal vein thrombosis after extended right hepatectomy and combined vascular resection and reconstruction which required immediate relaparotomy. This occurred in the patient with the poorest stent function and also the highest preoperative bilirubin despite the efforts for relief of jaundice and cholangitis with ERCP and PTD prior to surgery. According to the histology report, there was evidence of ascending cholangitis and microabscess formation within the liver parenchyma at a distance from the tumour. This finding is in agreement with the reported high risk of postoperative complications in cases with hilar malignancies and unrelieved jaundice prior to resection. However, it might be argued that hepatic artery resection and unrelieved jaundice should be considered as absolute contraindications for any attempt in such complex cases, especially if a right extended hepatectomy is the necessary type of resection.1214

Operating in the presence of endobiliary metallic stents represents a highly demanding surgical situation. Although not common, the option of revising the initial diagnosis in the presence of SEMS is indeed a reality, which probably will become more frequent in the future due to centralization of the complex hepatobiliary cases in high-volume surgical centres. Although hospital and surgeon procedure volume are well known to be independent factors associated with improved outcomes in complex HPB surgery,15,16 the importance of the available hospital clinical resources receives constantly more attention in the published literature. Joseph et al.17 has highlighted recently the interdependent relationship between hospital volume and the available clinical support system in achieving superior results in the field of pancreatic resections.

We consider the exposure of the surgical team in liver transplantation and specifically in living-donor-related transplants (LDLT), equally important in the management of these complex cases. Nguyen et al.18 demonstrated that volumes of liver transplant and partial hepatectomy procedures are strongly correlated with superior outcomes following liver resections for complex hepatocellular carcinoma cases. In accordance, surgical centres with extensive experience in living donor liver transplantation reported recently significantly improved results in 302 cases of hilar cholangiocarcinoma resected within a 7-year period, implementing the experience of LDLT in the surgical approach of these cases.19

The outcome of our case series might raise concerns regarding the benefit and the resource utilisation they demanded. However, despite the recent improvements in survival by non-surgical alternatives, R0 resection remains the mainstay among the therapeutic options with clear superiority regarding long-term outcome.20,21 We believe that “centralising” these complex surgical cases to high-volume tertiary centres with a dedicated HPB multidisciplinary team, prior to the application of any palliative measures, might result in the reduction of their occurrence.

Our concept is that, in the setting of malignant entities, the presence of metallic stents does not alter the plan of the radical resections needed to achieve a therapeutic outcome. In contrast, their application in benign conditions mimicking inoperable neoplasms upgrades the surgical demands at the level of oncological surgery. Since a significant rate of complications should be anticipated, a detailed multidisciplinary approach at a high level of expertise and resources should be at the basis of the management algorithm. As surgical resection is the only option for curative treatment of such cases, delaying the placement of metallic stents prior to evaluation at a referral surgical centre is the only option for avoiding this scenario.

Copyright information

© The Society for Surgery of the Alimentary Tract 2011