Abstract
Abstract
Background:
Laparoscopic-assisted extended hepatectomy and laparoscopic hepaticojejunostomy reconstruction can be performed for hilar cholangiocarcinoma by combining our existing protocols for laparoscopic anatomic hepatectomy and laparoscopic hand-sewn bilio-enteric anastomosis.
Subjects and Methods:
Our first patient was a 42-year-old man with cholangitis and jaundice from tumor obstructing the hepatic duct bifurcation who underwent a right extended hepatectomy for hilar cholangiocarcinoma (Bismuth IIIa), radical portal lymphadenectomy, and Roux-en-Y hepaticojejunostomy using laparoscopic techniques. A four-trocar, one 6-cm wound protector laparoscopic technique was used. Inflow and outflow exclusion was achieved first, followed by liver transection. Radical portal lymphadenectomy was performed. A Roux-en-Y hepaticojejunostomy was constructed laparoscopically. We have performed three other cases using the same technique: two requiring right extended hepatectomy and one requiring left extended hepatectomy.
Results:
No intraoperative complications occurred during the 4.0-hour procedure. Tumor margins were clear. The patient was given oral diet on Day 1 and discharged on Day 3 after surgery. No blood transfusions were necessary. A cholangiogram performed 10 days after surgery demonstrated patent hepaticojejunostomy, and magnetic resonance imaging performed during week 3 demonstrated the normal caliber of the intrahepatic biliary system. At 6 months, the patient was completely without symptoms and exhibited normal liver function tests.
Conclusions:
Laparoscopic-assisted right extended hepatectomy for hilar cholangiocarcinoma with laparoscopically hand-sewn hepaticojejunostomy in select patients can be achieved with good outcomes.
Introduction
T
Several liver centers have adopted a laparoscopic approach for segmental liver resections with very favorable outcomes, which include decreased length of hospital stay and accelerated recovery time. 4 Our center uses the same strategic approach for laparoscopic and open right extended hepatectomies, which typically begins with control of the cystic artery and the cystic duct (when the gallbladder is present), followed by right hepatic artery ligation and right portal vein ligation. We then perform full mobilization of the right lobe of the liver, followed by hepatic vein ligation. The final step is parenchymal transection. The laparoscopic approach is our preference for right hepatectomies because of its superior anatomic views of the hilar plate, portal pedicles, hepatocaval attachments, and the hepatic vein. The benefits include smaller midline incisions and shorter hospital stays. In this report, we used our standard protocol for formal anatomic right liver resections to perform a hilar tumor resection with hand-sewn bilioenteric reconstruction. We believe this is the first such report of a laparoscopic Klatskin's tumor resection and laparoscopic reconstruction.
Subjects and Methods
Patients
The first patient was a 42-year-old Hispanic man who developed jaundice and cholangitis. Magnetic resonance imaging demonstrated dilated left biliary radicals and a 1.8-cm-diameter tumor of the right hepatic duct at the confluence (Fig. 1). Because of the small size of the left liver lobe, a percutaneous transhepatic cholangiocatheter was placed to decompress the left biliary system, and the anterior and posterior branches of the right portal vein were embolized to induce left lobe hypertrophy (Fig. 2). The embolization was done individually on the secondary branches of the right portal vein to keep the subsequent inflammatory process away from the hilum. The patient was allowed 4 weeks of recovery from sepsis prior to surgical resection.


Percutaneous transhepatic cholangiogram and catheter placement through the left lobe of the liver. Embolization coils were placed in the anterior and posterior branches of the right portal vein to induce left liver hypertrophy.
After the first patient, we have performed three other laparoscopic resections for hilar cholangiocarcinoma (two right hepatectomies and one left hepatectomy).
Position and instruments
The patient is placed in the supine position with both arms abducted at 90° from the torso. A urinary bladder catheter is placed. The table is tilted 30° to the left and in a 30° reverse Trendelenburg position (Fig. 3). Standard laparoscopic dissecting instruments are used. The LigaSure™ device (Valley Lab, Covidien, Norwalk, CT) is used to ligate small vessels. Harmonic® ultrasonic shears (Ethicon, Cincinnati, OH) are used to divide the liver capsule and for parenchymal transection. Vascular, bowel, and gray load EndoGIA™ cutting staplers (Covidien) are used to divide major vessels within the liver parenchyma. The Gelport™ (Applied Medical, Rancho Santa Margarita, CA) is placed in the upper midline through a 6-cm incision to assist in retraction, specimen removal, and formation of the Roux limb. A 30° laparoscope is used.

Patient position using four trocars in the upper abdomen (10-mm subxiphoid, midclavicular, anterior axillary, and a 5-mm midaxillary). A 6-cm protected supraumbilical incision is used for the Gelport and specimen removal.
Operative procedure
There are two surgeons, one on each side of the patient. The surgeon on the left places one hand through the Gelport and operates through the subxiphoid trocar. The assistant surgeon on the right operates the camera. Hepaticojejunostomy and lymphadenectomy are performed from the patient's right side. As is usual for liver resections, fluid restriction is maintained during the procedur to decrease central venous pressure. The resection is conducted using the following sequence:
1. Transection of the distal common bile duct with laparoscopic scissors, elevation of the proximal stump of the bile duct, and ligation of the right hepatic artery using a tie-and-LigaSure technique (Fig. 4A). The right portal vein is divided using the vascular EndoGIA (Fig. 4B). This results in vascular inflow control and ischemic demarcation of the right lobe. 2. The triangular and the coronary ligaments of the right liver lobe are released with electrocautery. The anterior surface of the inferior vena cava is cleared from the small venous perforators using the LigaSure device from the hilum of the liver toward the right hepatic vein. The right hepatic vein is dissected free and divided using the vascular load EndoGIA stapler (Fig. 5). 3. Liver transection is performed first by entering the hepatic capsule to the left of the ischemic demarcation line, close to the umbilical fissure; typically, the gallbladder is left in situ and used for retraction. The parenchyma is divided using ultrasonic shears. The major vessels are divided with either white or gray EndoGIA staplers. The caudate process is removed. Once the liver parenchyma is fully divided, the right liver, hepatic duct, and common bile duct are divided en bloc from the left hepatic duct using cautery scissors. In this patient, the previously placed left hepatic stent catheter assisted in the identification of the left hepatic duct (Fig. 6). Portal lymphadenectomy begins from the common hepatic artery toward the portal vein medially and then posteriorly to harvest the portal lymph nodes. Finally, the lymphadenectomy clears all the soft tissue anterior to the porta hepatis, between the hepatic artery and bile duct. The liver specimen is removed through the protected midline incision (Fig. 7). The distal common bile duct and the left hepatic duct are checked for tumor margins. The Roux limb is created through the protected incision prior to reestablishing pneumoperitoneum. 4. A small enterotomy is created in the proximal end of the Roux limb, and the hepaticojejunostomy is formed using 4-0 polyglactin 910 (Vicryl®; Ethicon) suture in running continuous fashion (Fig. 8). The percutaneous stent is left across the anastomosis and flushed with saline to assure there is no bile leak. A drain is placed in the right upper quadrant.





Only the midline Gelport fascia required closure. All skin incisions were closed using absorbable subcuticular sutures. The patient had the On-Q® pump (I-Flow Corp, Lake Forest, CA) placed in the prefascial space for analgesia. The first operation was completed in 4.0 hours, with less than 100 mL of blood loss. The liver transection was done without the use of the Pringle maneuver or dividing the falciform ligament. All 3 remaining cases were also performed in less than 4.0 hours. None of the patients required blood transfusions. There were no intraoperative or postoperative complications.
Results
The patient was started on a diet on the first postoperative day and discharged on postoperative Day 3 with oral analgesics. The specimen margins were negative for tumor. A pull-back cholangiogram performed 10 days after surgery showed an intact and patent hepaticojejunostomy with no biliary dilatation (Fig. 9A). The biliary catheter was removed. The patient had normal liver function test values at 2 weeks after surgery and at 6 months follow-up (Fig. 9B). The other 3 patients also had negative margins on pathology and were discharged within 4 days.

Discussion
Our cases demonstrate the feasibility of a minimally invasive technique for hilar cholangiocarcinoma resection. This approach takes advantage of the current skills for laparoscopic major hepatectomy and hilar dissection using standard laparoscopic instrumentation. For major hepatectomies, we prefer complete dissection of the porta hepatis and vascular inflow and outflow control prior to liver transection. The operative time and the extent of the laparoscopic dissection compare favorably with the results of the largest open surgical series reported for hilar cholangiocarcinoma, 5 with the primary difference being the location and extent of incision. Classically, an extended right subcostal or a chevron incision is standard for this operation. Such an incision not only increases the surgical trauma and postoperative recovery time but also increases the evaporative water loss with subsequent increase in intravenous fluid administration. By choosing the laparoscopic approach, not only are the incision complications minimized, but also the quality of visualization is significantly enhanced, leading to greater precision in the control of vascular structures. With this case, pain control was achieved with use of an On-Q pump and oral analgesics, with no patient-controlled analgesia infusion or epidural catheter infusion. None of the patients required transfusion of blood products, and all patients were able to be discharged by postoperative Day 4. These represent the collective effects of reduced operative trauma.
These cases also illustrate how laparoscopic surgery is surmounting the technical challenges of hepatobiliary–pancreatic surgery. Hilar cholangiocarcinoma resections are perhaps the most difficult hepatic operation after liver transplantation. The operation involves a major liver resection and biliary reconstruction. Both resection and biliary reconstruction have been described laparoscopically to some extent, but their combination is certainly unique. The liver resection demonstrated in this case is different because the portal dissection begins by transecting the distal bile duct and dissecting proximally toward the confluence. This approach is typically not difficult unless confronted with a very close tumor creating a significant desmoplastic reaction that obliterates the identification of vasculobiliary structures.
In general, a minimally invasive approach will always be preferred. This has been demonstrated historically when laparoscopic cholecystectomy was favored over the open procedure, in spite of a higher incidence of bile duct injury. 6 Hepatobiliary surgeons should be prepared to confront this challenge and embrace these techniques for benefit to patients.
Another advantage of the laparoscopic approach is already used in our practice. If it is anticipated that hilar dissection cannot be completed laparoscopically, the trocar placements permit full mobilization of the right lobe of the liver, including dissection of the right hepatic vein. Once these steps are completed, we simply extended the midline hand-port incision vertically toward the xiphoid and complete the resection, avoiding a major right subcostal or chevron incision. By using this approach, even patients who are not amenable to full laparoscopic right liver resections can benefit from some aspect of the minimally invasive approach.
A final advantage of the laparoscopic approach is the preliminary exploration of the abdominal cavity before embarking on major explorations. Prospective data from Memorial Sloan-Kettering Cancer Center showed that laparoscopy identified metastatic disease at the time of surgery in 35% of patients with hilar cholangiocarcinoma. 7
Contraindications to this technique include the presence of a tumor extremely close to the contralateral hepatic artery or portal vein, unless the surgeon wishes to take advantage of laparoscopic right hepatic lobe mobilization.
The authors believe that this technique does not require any need for additional or sophisticated equipment. Indeed, standard technology and instruments are sufficient to perform hepatobiliary resection for the treatment of hilar cholangiocarcinoma.
There is little doubt that the laparoscopic approach offers enhanced views of the portal structures. As surgeons become more familiar with hilar dissection using this technique, the current challenges for vascular control will soon be overcome. Currently, even though the lead author is a classically trained (open) hepatobiliary surgeon, 80% of hepatic resections are performed laparoscopically in the group's practice. All cases are completed with extrahepatic dissection of individual portal structures, inferior vena cava, and hepatic veins. Although we do not believe that these techniques are easily adoptable, major centers that have already embarked on laparoscopic hepatectomies should incorporate these innovations.
In the first case, the caudate lobe was not completely resected because the tumor was to the right of the confluence, and we found the caudate duct originating from the left hepatic duct. This is a very unusual pattern because the caudate lobe resection should be an integral part of the operative management of hilar cholangiocarcinoma. 8
In summary, we believe that the laparoscopic approach to the management of hilar cholangiocarcinoma is feasible, and its utilization will increase as surgeons become more facile with laparoscopic hepatic resections.
Footnotes
Disclosure Statement
No competing financial interests exist.
