Preoperative Endoscopic Ultrasound-Guided Hepaticogastrostomy for Definite Biliary Drainage in Hilar Cholangiocarcinoma Laparoscopic Resection: A Hybrid Minimal-Invasive Technique

Abstract

Background and study aims

Laparoscopic approach of perihilar cholangiocarcinoma (PHC) is still challenging. We report the original use of a endoscopic hepaticogastrostomy (EHG) for definite biliary drainage in order to avoid biliary reconstruction.

Patients and methods

A 70-year-old man presenting with jaundice was referred for resection of a Bismuth type IIIa PHC. Repeated endoscopic retrograde cholangiopancreatography failed to drain the future liver remnant, enabling only right anterior liver section drainage. EHG was performed three weeks before surgery. A hepatogastric anastomosis was created, placing a half-coated self-expanding endoprosthesis between biliary duct of segment 2 and the lesser gastric curvature.

Results

A laparoscopic right hepatectomy extended to segment 1, common bile duct, and hepatic pedicle lymphadenectomy was performed. The left hepatic duct was sectioned and ligated downstream to the biliary confluence of segment 2-3 and 4 allowing exclusive biliary flow through the EHG. The patient was disease free at 12 months, postoperative outcomes were uneventful except three readmissions for acute cholangitis due to prosthesis obstruction.

Conclusions

EHG may be used as definite biliary drainage technique in laparoscopic PHC resection, at the expense of prosthesis obstruction and cholangitis.

Introduction

Perihilar cholangiocarcinoma (PHC) is a rare but aggressive biliary duct cancer of either the extrahepatic main biliary confluence or intrahepatic small bile ducts adjacent to the biliary confluence and invading the hepatic hilum. ¹ Radical resection is the only intent to cure treatment but is characterized by a complex surgical management requiring major liver resections with biliary reconstructions.^1,2 It is thus generally admitted that open surgery is the standard of care and the postoperative course is consequently often complicated, with severe morbidity (27.5%-54%) and mortality rates (18%). ² Moreover, 5-year patient survival rarely exceeds 35%. ³

Recent technological innovations, improvement of surgical skills and growing surgical expertise in minimally invasive surgery have improved the feasibility and safety of laparoscopic extended liver resections as well as outcomes. ⁴ However, laparoscopic liver surgery is still a matter of debate in the field of PHC as its potential benefits are limited by the need to perform complex biliary reconstructions. ⁵

On the other hand, endoscopic advances in preoperative biliary drainage and in particular extraanatomical bile duct stenting (EABS) have opened up the horizons of complex minimal invasive treatments. Transmural intrahepatic biliary drainage/endoscopic ultrasound (EUS)-guided hepaticogastrostomy has recently been described as an effective alternative to percutaneous biliary drainage (PBD) in unresectable malignant biliary obstruction in case of Endoscopic retrograde cholangiopancreatography (ERCP) drainage failure. ⁶ Inspired by this armamentarium of novel endoscopic techniques and driven by the need to overcome laparoscopic biliary reconstruction difficulties but also postoperative anastomotic fistulas, we supposed that EUS-guided hepaticogastrostomy (EHG) could serve as an alternative to a hepaticojejunal anastomosis for definite biliary drainage. We present herein an original case of a laparoscopic right hepatectomy extended to segment 1 and main biliary confluence, ⁷ after EUS-guided hepaticogastrostomy for a Type IIIa Bismuth-Corlette (BC) PHC. ⁸ Bilioenteric continuity was exclusively provided by the preoperative endoscopic hepaticogastrostomy.

Patients, Material and Methods

A 70-year-old man with a body mass index of 27 kg/m² and a past surgical history of a midline laparotomy for a perforated duodenal ulcer was referred to our center for a recently diagnosed PHC. On MRI-MRCP and CT-scan, a 12 × 9 mm tumor was located on the main biliary confluence including both anterior and posterior right biliary ducts (type IIIa BC PHC). No vascular invasion or secondary lesions were observed and there were no signs of chronic liver disease. A right hepatectomy extended to segment 1, main biliary confluence and extrahepatic bile duct (H15678-B) associated with an extended lymphadenectomy of the hepatoduodenal ligament was decided and validated on a multidisciplinary oncological meeting. The ratio of the future liver remnant volume (FLRV)/total liver volume (TLV) was estimated at 36% (FLRV:680 mL/TLV: 1880 mL) and in the absence of a chronic liver disease, right portal vein embolization was judged unnecessary.

Repeated trans-papillary endoscopic biliary drainage failed to drain the future liver remnant (segments 2, 3 and 4), enabling biliary drainage only of the right anterior liver section. An EUS-guided hepaticogastrostomy was thus performed 3 weeks before surgery, allowing a complete normalization of liver function tests and jaundice. Informed written consent was obtained.

Results

Endoscopic Technique

EUS-guided transmural/transgastric hepaticogastrostomy (EHG) was performed using a therapeutic linear array echoendoscope (Linear Ultrasound Endoscope TGF-UC180J - Olympus Europa) under general anesthesia. Prophylactic antibiotic therapy (Cefazoline 1 gr IV) was administered prior to the endoscopic procedure. The intrahepatic biliary ducts within the left lobe were firstly visualized with an endoscopic ultrasound imaging in order to confirm feasibility of the technique and a color doppler ultrasound was used to verify the absence of vascular structures in the potential puncture trajectory. The segment’s 2 enlarged biliary duct (diameter ≥6 mm) was punctured using a 19G needle (EchoTip® Ultra HD Ultrasound Access Needle, Cook) under endosonographic control. Bile content aspiration confirmed intraductal position of the needle. A contrast agent was then injected under fluoroscopic control to obtain an antegrade cholangiogram of segments 2, 3 and 4. Subsequently, a rigid .035-inch guidewire (Jagwire 450 cm .035, Boston Scientific) was introduced through the needle lumen into the bile duct, but no passage was through the tumoral stricture. The position of the guidewire was maintained and a hepaticogastric fistula was established using a 6 Fr cystostome (EndoFlex, Boucart. Medical). Next, a half-coated self-expanding endoprosthesis (Hanarostent, 10 × 80 mm, Olympus Europa) was introduced under endosonographic and fluoroscopic guidance through the subcardial region of the lesser gastric curvature and segment’s 2 biliary duct. A double pigtail plastic stent was placed through the stent to ensure permeability (Solus® Double Pigtail Stent 10 cm 7 Fr, Cook) Finally, a contrast cholangiography through the endoprosthesis confirmed correct biliary drainage of all three segments and the absence of any leaks. The forementioned technique is reported in Video 1.

Surgical Technique

Hepatic Pedicle Dissection and Lymphadenectomy

The abdominal cavity was thoroughly inspected to exclude any tumoral peritoneal seeding. The first step consisted in performing an adhesiolysis in order to restore anatomical landmarks. Left liver mobilization was not performed and the inter-hepaticogastric space was not dissected to preserve the hepaticogastric fistula and avoid displacement or migration of the endoprosthesis. Dissection of the left hepatic artery confirmed absence of tumoral invasion. Next, the right hepatic artery was dissected, controlled and sectioned. The distal common bile duct (CBD) was sectioned just above the duodenum permitting extraction of the plastic biliary stent, sent for bacterial culture analysis. The distal end of the CBD was finally clipped, and its proximal end sent for frozen section analysis. Anterior traction of the CBD facilitated portal vein dissection and lymphadenectomy. Finally the right portal branch was dissected free, taped and sectioned between clips.

Hepatectomy Phase

The right triangular ligament was sectioned and the right liver lobe was completely mobilized. The main portal fissure was then progressively opened along the right edge of the middle hepatic vein and in direction to the Arantius groove using a Thunderbeat® device (Olympus Europa). Once the parenchymal transection reached the roof of the left hepatic duct, the latter was sectioned downstream to the junction of segments’ 2-3 and 4 biliary ducts (B2-3-4). A frozen section analysis of the left hepatic duct was performed once the liver specimen was removed. Section of the left hepatic duct enabled access to the Arantius groove and section of the Arantius ligament in its confluence with the left hepatic vein. The dorsal sector of the liver was finally detached from the inferior vena cava after sectioning of the small Spigelian veins and division of the right hepatic vein using endovascular stapler (Vascular 35 mm, Ethicon, France). The right liver was finally extracted in a plastic bag through a Pfannenstiel incision. Finally, the left hepatic duct was suture ligated allowing exclusive biliary flow through the hepaticogastric fistula. Bleeding and bile leak of the cut liver surface were secured. Overall blood loss was 200 mL and no drain was left in place at the end of the procedure. The forementioned technique is reported in Video 2.

Postoperative and Long-Term Outcomes

The patient received oral feeding on postoperative day (POD) 0. Computed tomography scan on POD 5 showed a homogenous liver parenchyma, patent vessels, no fluid collection and no biliary duct dilatation. The postoperative course was uneventful and the patient was discharged on POD 6. Histopathologic analysis revealed a 15 mm well differentiated T2bN0 cholangiocarcinoma with 6 lymph nodes harvested and negative (R0) resection margins. The patient received 6 months of postoperative capecitabine. ⁹ The patient was readmitted at 2, 3 and 4 months for an acute cholangitis related to an endoprosthesis obstruction necessitating replacement. Finally, the endoprosthesis was definitively removed at 5 months postoperative, and no recurrent episodes of acute cholangitis were observed ever after. We assumed that food impact leading to obstruction might be more frequent in a large prosthesis lumen rather than in a smaller hepatico-gastric communication maintained by the continuous anterograde bile flow. At 12 months follow up, the patient was doing well, had normal liver function tests and no evidence of local or distant recurrence.

Discussion

To our knowledge, this is the first report of a laparoscopic right hepatectomy extended to segment 1 and main biliary confluence after EUS-guided hepaticogastrostomy for PHC. In 1947, Longmire first described the procedure of peripheral intrahepatic cholangiojejunostomy, in the setting of a reoperation for a common bile duct transection after a primary choledochojejunostomy had also strictured. His technique involved the anastomosis of a Roux-en-Y jejunal loop to a dilated intrahepatic duct, exposed by partial resection of the left hepatic lobe, allowing decompression of the biliary tree under condition of an intact biliary bifurcation allowing for right to left intrahepatic duct bile drainage. ¹⁰ Since then, his technique has been described for surgical treatment of biliary strictures but also palliation for malignant bile duct irresectable tumours of the liver hilum. In the present case, minimally invasive strategies derived from endoscopic extraanatomical bile duct stenting and laparoscopic liver surgery were combined together to overcome intraoperative laparoscopic biliary reconstruction difficulties but also avoid postoperative hepaticojejunal anastomotic fistulas. Indeed, technically radical resection of PHC requires advanced laparoscopic skills and experience in laparoscopic major liver resection with caudate lobectomy, hepatoduodenal lymphadenectomy and anastomosis between the hepatic duct and jejunum.

In recent years, improvement of surgical skills and growing surgical expertise in minimally invasive surgery have improved the feasibility and safety of laparoscopic extended liver resections as well as patient outcomes.^4,11 However, in the particular setting of PHC, biliary reconstruction can be challenging in laparoscopy, especially in the case of small ducts or multiple ductal anastomoses. Though introduced more recently, robot-assisted liver surgery, commonly practiced nowadays, ¹² has the well-known advantages of a 3D view and more flexible movements ¹³ facilitating minimally-invasive hepatico-jejunostomies even in presence of multiple ducts. However, robot-assisted liver resections compared to laparoscopic procedures are associated with longer operative time and total cost,^14,15 while robot is not widely available. Since, there is still a substantial shortage of evidence clearly addressing the issue of which specific liver procedure is worth managing with a robotic approach we supposed that a hybrid endoscopic-laparoscopic strategy would overcome this technical obstacle.

Furthermore, we supposed that an additional advantage of the EHG would be to avoid a hepaticojejunal anastomosis and thus decrease the risk of postoperative anastomotic fistulas that is reported to be as high as 16.5%-33%.^16,17 EHG has recently been described as an effective and alternative method to percutaneous biliary drainage (PBD) in unresectable malignant biliary obstruction in case of endoscopic retrograde cholangiopancreatography (ERCP) failure. ¹⁸ Technical success rate of this technique has been described to be as high as 98% and common adverse events are most commonly bleeding (4.03%), bile leakage (4.03%), stent migration (2.68%) and cholangitis (2.43%). ¹⁹ On the other hand, compared to conventional percutaneous biliary drainage EABS is characterized by similar technical and clinical success rates and significantly lower complication rates compared with the external drainage group as demonstrated in a systematic review and meta-analysis of nine studies. ²⁰

Our approach is a first step towards simplifying technically an already complex laparoscopic surgical procedure for PHC. This first reported strategy however needs to be evaluated in centers with extensive experience in both laparoscopic liver surgery and advanced endoscopy-guided biliary drainage. Moreover, appropriate patient selection plays an important role to safely continue the development of hybrid endoscopic-laparoscopic liver surgery procedures. In our case, no tumoral vascular extension existed and thus arterial or portal vein reconstruction, which may be associated in up to 38% of PHC liver resections, ²¹ was not needed. Finally, an important technical point in this patient is that the EHG performed through the segment’s 2 biliary duct provided biliary drainage for all 3 left liver segments as the biliary confluence of segments 2,3 and 4 was intact. Since the secondary biliary confluence was more than 2 cm away from the tumor, section of the left hepatic duct was possible without interruption of the B2-3-4 confluence. If however, multiple biliary ducts were present in the section area, a hepatico-jejunal anastomosis would have been necessary in order to efficiently drain the left liver. In the same manner, performing this hybrid minimal-invasive technique after a right hepatectomy extended to segments 1 and 4 (H145678-B) would have necessitated an intact B2-B3 biliary confluence. Finally, permanent biliary flux through the EHG permitted removing the endoprosthesis after 2 months without any risk of fistula closure and thus avoiding common prosthesis complications like obstruction and cholangitis. Our patient did not present any biliary reflux disease or obstructive jaundice during follow-up.

In conclusion, this hybrid endoscopic-laparoscopic approach for treatment of a type IIIa BC PHC can be attempted in highly selected recipients and by surgical and endoscopic teams with significant expertise. Even though the clinical benefit of our approach cannot be evaluated on the basis of this single case, additional experience is needed before any solid conclusions can be drawn.

Supplemental Material

Supplemental Material