Overview

Our recent approach to perihilar cholangiocarcinoma has gradually changed, from the very detailed preoperative percutaneous transhepatic biliary drainage (PTBD), cholangioscopy, and vascular imaging to multidetector-row computed tomography (MDCT) and three-dimensional CT angiography that facilitates sufficient assessment of tumor extension and staging to selective endoscopic nasobiliary drainage (ENBD), only for the future remnant liver. When cholangiography provides insufficient information of the tumor extent, or segmental cholangitis develops, additional PTBD should be applied to the undrained bile ducts. In this chapter we introduce a recently developed “Japanese” extended resection for difficult perihilar cholangiocarcinoma that might differ from the Western approach.

Preoperative Diagnosis and Management of Hilar Cholangiocarcinoma

Accurate preoperative staging using extensive investigation is indispensable prior to radical resection for hilar cholangiocarcinoma (Nagino et al, 1998; Nimura, 1994, 1997; Nimura et al, 1990a, 1995b, 2000). Most cases of hilar cholangiocarcinoma are associated with jaundice as a result of obstruction of the proximal bile ducts, either within or outside of the liver. Obstruction usually involves multiple ducts as a result of proximal spread of carcinoma along the intrahepatic segmental bile ducts. Multiple applications of PTBD (Nagino et al 1992; Nimura et al 1995a; Takada et al 1976) to relieve the cholestasis and restore the functional reserve of the future remnant liver, we believe, is essential prior to operation involving extensive hepatic resection.

In the third edition of this text, we explained that the first step in the preoperative management of hilar cholangiocarcinoma was PTBD; however, MDCT is taken before biliary drainage to define which side of the liver should be resected, and PTBD applied by the direct anterior approach under fluoroscopic guidance (Takada et al, 1976) or ENBD for the future liver remnant (FLR) are selected to relieve cholestasis of the FLR. This offers both diagnostic and therapeutic advantage (Nagino et al, 1995a), and it minimizes PTBD sessions and the number of PTBD catheters. On the other hand, magnetic resonance cholangiopancreatography (MRCP) is occasionally insufficient to diagnose the difficult local anatomy of the separated intrahepatic segmental and/or sectoral ducts and to design an appropriate operative procedure, especially in patients with Bismuth type III or IV tumors (Bismuth & Corlette, 1975). In such cases, high-quality cholangiograms through the PTBD catheters, taken in various positions—supine, right and left anterior oblique, right and left lateral, and cephalad-anterior-oblique positions (Kamiya et al, 1994)—often clearly demonstrate the tumor location and provide the most reliable information on the proximal extension of hilar cholangiocarcinoma along the intrahepatic segmental bile ducts (Ebata et al, 2002; Sakamoto et al, 1998; Fig. 90C.1).

FIGURE 90C.1 A cholangiogram through four percutaneous transhepatic biliary drainage catheters (arrows) shows stricture at the hepatic hilum and suggests cancer extension along the intrahepatic segmental bile ducts (arrowheads). Numerals refer to the Couinaud’s segments of the liver: 8b is a lateral branch of the right anterior superior segmental bile duct, and 8c is a dorsal branch of the right anterior superior segmental bile duct.

When cholangiography provides insufficient information on the tumor extent, additional PTBD is performed to the undrained bile ducts. After dilating the sinus tract of PTBD, percutaneous transhepatic cholangioscopy (PTCS) can also provide reliable information on anatomic variations of the biliary tree and mucosal extension of the cancer (Kamiya et al, 1994; Nimura, 1993; Nimura et al, 1989). Superficial mucosal extension of the carcinoma is often associated with polypoid and/or nodular tumors of a macroscopic type (Igami et al, 2009). Thus PTCS or per oral cholangioscopy with biopsy may be valuable in diagnosis of the extent of cancer (Itoi et al, 2000, 2007; Nimura et al, 1988; Sakamoto et al, 1997). On the other hand, coexistence of biliary tract infection negatively affects the functional reserve of the liver. When intrahepatic segmental cholangitis develops, even in patients with PTBD catheters during preoperative period, urgent additional selective PTBD to the affected segmental duct should be performed (Kanai et al, 1996; Fig. 90C.2).

FIGURE 90C.2 Percutaneous transhepatic biliary drainage (PTBD), to the right anterior sectoral ducts performed for intrahepatic segmental cholangitis. 5, A branch of the right anterior inferior segmental bile duct; 8a, a ventral branch of the right anterior superior segmental bile duct.

Concomitant vascular resection and reconstruction is indicated in some advanced cases of hilar cholangiocarcinoma (Nimura et al, 1991). We previously performed visceral angiography, percutaneous transhepatic portography, and selective retrograde hepatic venography to assess the vascular invasion of the tumor (Nishio et al, 1999, 2003). Recently, three-dimensional images of MDCT using techniques of volume rendering, multiplanar reformation, and maximum intensity projection have taken over because of the high-quality images and reduced invasiveness (see Fig. 90C.13). We usually estimate the relationship between a tumor and the vascular system in the liver and hepatoduodenal ligament and diagnose the vascular involvement of the tumor on the multiplanar reformatted images; we plan the methods of resection and reconstruction—wedge or segmental resection, direct end-to-end anastomosis, or segmental auto vein grafting—by volume-rendered images and maximum-intensity projection images (Senda et al, 2009; Sugiura et al, 2008).

FIGURE 90C.13 Three-dimensional reconstructed images of multidetector-row computed tomography. A, Coronal view of multiplanar reformatted images shows left hepatic duct tumor invading the portal bifurcation (arrow). B, Anteroposterior view of volume-rendered image demonstrating obstruction of the left portal vein and narrowing of the contralateral side of the portal bifurcation (arrow). Portal vein resection was planned along the lines shown. C, Craniocaudal view of maximum-intensity projection image reveals narrowing of the portal bifurcation (arrow). This view cannot be obtained by conventional arterial portography or percutaneous transhepatic portography.

Postoperative morbidity and mortality rates remain considerable, particularly if extensive resection is necessary (Nagino et al, 2001). Postoperative liver failure sometimes occurs and results in death. For this reason, liver resection is usually scheduled only after the liver has been decompressed and the serum total bilirubin concentration falls below 2 mg/dL. In addition, since 1989, we have routinely performed percutaneous transhepatic portal vein embolization (PVE) (Nagino et al, 1993, 1996, 2000, 2006a) as preoperative preparation for extensive liver resection. This is done to minimize the incidence of postoperative liver failure. After estimation of the resultant compensatory hypertrophy by volumetric CT scan (Nagino et al, 1995b, 1995c) and of the functional reserve of the liver as assessed by the indocyanine green clearance rate (Uesaka et al, 1996), hepatectomy is performed, usually 2 to 3 weeks after PVE. A Japanese series implemented a management strategy for patients with hilar cholangiocarcinoma that consisted of preoperative biliary drainage, PVE, and major hepatobiliary resection; it reported a 0% mortality rate in more than 100 consecutive cases (Sano et al, 2006).

Impaired intestinal barrier function does not recover with PTBD without bile replacement, which can restore the intestinal barrier function during external biliary drainage in patients with biliary obstruction, primarily as a result of repair of physical damage to the intestinal mucosa. Thus, in patients with hilar cholangiocarcinoma and external biliary drainage, we routinely replace bile prior to operation (Kamiya et al, 2004; Kanazawa et al, 2005). Also, perioperative administration of synbiotics can enhance immune responses, attenuate systemic postoperative inflammatory responses, and improve the intestinal microbial environment (Sugawara et al, 2006). These procedures may reduce postoperative infectious complications after major hepatobiliary resection in difficult patients with hilar cholangiocarcinoma.

Right Hepatic Resection with Total Caudate Lobectomy, Extrahepatic Bile Duct Resection, and Portal Vein Resection and Reconstruction

Right hepatectomy with total caudate lobectomy is carried out for tumors involving the right anterior and posterior sectoral bile ducts, with sparing of the left medial segmental bile duct to segment IV, or when the right hepatic artery is also involved (see Chapters 50B and 90B). If the cancer involves the right hepatic duct and the left medial segmental duct, anatomic right hepatic trisectionectomy with caudate lobectomy is indicated (Nagino et al, 2006b).

At operation and after exploration of the peritoneal cavity, PTBD catheters are fixed at the liver surface to maintain intraoperative biliary drainage. The right lobe is often atrophic to some extent, and a faint demarcation between the right and left lobe is observed as a result of the preoperative PVE.

After retropancreatic lymph node dissection, the distal bile duct is divided above the pancreas with a histologic free margin; the hepatoduodenal ligament is dissected, and the vessels are skeletonized and removed (Bhuiya et al, 1992). The middle hepatic artery usually runs ventral to the left portal vein and enters the liver below the left medial segment branch of the portal vein; this artery is carefully preserved. The left hepatic artery enters the liver to the left of the umbilical portion of the portal vein (Figs. 90C.3 to 90C.5).

FIGURE 90C.3 A schematic illustration after skeletonization of the hepatoduodenal ligament is shown. A catheter is inserted from the distal stump of the common bile duct for intraoperative biliary drainage (arrow).

FIGURE 90C.4 A schematic illustration just prior to resection of the left intrahepatic sectoral ducts. The right liver and caudate lobe are extracted to the right side. The resection line is indicated by double lines.

FIGURE 90C.5 Intraoperative image during a right hemihepatectomy with caudate lobe resection showing complete skeletonization of the hepatoduodenal ligament. Regional lymph nodes and connective tissues (arrowheads) are dissected en bloc. The transection line of the liver parenchyma (solid line) and the resection point of the left intrahepatic ducts (dotted line) are shown. The right portal vein (RPV) is transected at its origin with transverse suture closure. MHA, middle hepatic artery; LHA, left hepatic artery.

Following skeletonization of the hepatoduodenal ligament, preparation of the caudate lobe is carried out by isolation, ligation, and division of the arterial branches and portal branches of the caudate lobe. The details of the technique are described above (Figs. 90C.3 to 90C.7; see also Fig. 90C.12). Although the arterial branches directly arise from the left and right hepatic arteries, they cannot be accurately identified in some cases. Two to six branches of the portal vein arise from the left portal vein, two to three branches arise from the right portal vein, and one to two branches arise from the main trunk or the bifurcation of the portal vein.

FIGURE 90C.6 An intraoperative view of a right hemihepatectomy with caudate lobe resection depicts a view just prior to bile duct resection. The dotted line shows resection point of the left intrahepatic sectoral ducts.

FIGURE 90C.7 Intraoperative view after right hepatectomy with total caudate lobectomy; extrahepatic bile duct resection is demonstrated. Hepaticoplasty is done for left hepatic segmental and/or subsegmental ducts. B4a, transected inferior branch of the left medial segmental bile duct; B4b, transected superior branch of the left medial segmental bile duct; B2+3, the left lateral sectoral bile duct; IVC, inferior vena cava; MHV, middle hepatic vein.

FIGURE 90C.12 Intraoperative image after a right hepatectomy with total caudate lobectomy, extrahepatic bile duct resection, and portal vein (PV) resection and reconstruction. The PV reconstruction is done by end-to-end anastomosis. The left medial hepatic artery (A4) originates from the right hepatic artery, which has been divided. B2+3, transected left lateral segmental bile duct; B4, transected left medial segmental bile duct; A2+3, left lateral sectoral hepatic artery; MHV, middle hepatic vein; RHA, right hepatic artery.

The significance of total caudate lobectomy in cases of hilar cholangiocarcinoma is, of course, not resection of the parenchyma of the caudate lobe but clearance of the connective tissue of the hilar plate around the caudate bile duct branches, which are often involved by cancer (Nimura et al, 1990). After complete division of the caudate arteries and portal vein branches, the right hepatic lobe is mobilized, and short retrohepatic veins are ligated and divided. The caudate lobe is completely detached from the inferior vena cava (IVC) as described above, and the confluence of the right hepatic vein (RHV) with the IVC is carefully encircled, clamped, divided, and closed with a running suture or a vascular stapler.

In case of direct cancer invasion of the portal bifurcation, portal vein resection and reconstruction is performed prior to liver resection (Figs. 90C.8 to 90C.12). Direct end-to-end anastomosis of the main trunk of the portal vein and the left branch is carried out (Ebata et al, 2003; Nimura et al, 1991; see Chapter 91B). Portal vein resection and reconstruction is carried out during the hilar dissection prior to hepatic parenchymal transection, because the portal flow to the FLR is easily impeded as a result of kinking during operative manipulations. Direct end-to-end anastomosis between the main portal trunk and the left portal vein is usually possible during right-sided resections (Kondo et al, 2003). On the other hand, interposition of an autogenous vein graft is often required during portal vein reconstruction, between the right portal vein and the main trunk during left-sided resections (Figs. 90C.9 to 90C.15). We usually harvest an external iliac vein for an autogenous vein graft by an extraperitoneal approach. The key to portal vein resection and reconstruction during right-sided hepatectomy is the feasibility of cross clamping the root of the umbilical portion of the left portal vein. In the case of left hepatectomy, isolation and clamping of the right posterior sectoral and/or the right anterior sectoral portal vein are key maneuvers.

FIGURE 90C.8 Schematic illustration of portal vein resection and reconstruction by end-to-end anastomosis during right hepatectomy. After stay sutures are placed at both edges (A), the intraluminal technique is used for the posterior wall suture (B), and over-and-over sutures are placed for the anterior wall (C).

FIGURE 90C.9 Schematic illustration of portal vein resection and reconstruction using a right external iliac vein graft during left hepatic resection. First, the distal anastomosis between the right portal vein and the graft is performed using an over-and-over technique for both sides with 6-0 prolene. Next, stay sutures at both edges are placed, and the proximal side anastomosis between the vein graft and the main portal vein is performed with intraluminal technique for the posterior wall suture; an over-and-over technique is used for the anterior wall with 6-0 or 5-0 prolene. RHA, right hepatic artery.

FIGURE 90C.10 An intraoperative image during a right hemihepatectomy shows tumor involvement of the portal vein. LPV, left portal vein; LHA, left hepatic artery; PV, main portal vein; GDA, gastroduodenal artery.

FIGURE 90C.11 Intraoperative view during a right hemihepatectomy shows portal vein resection and reconstruction with an external iliac vein (arrowheads). In many cases of right hepatobiliary resection, portal vein (PV) resection and reconstruction with or without an interposition graft is performed prior to liver parenchymal transaction. LPV, left portal vein; LHA, left hepatic artery; GDA, gastroduodenal artery.

FIGURE 90C.14 Schematic illustration during an extended left hepatic resection, caudate lobectomy with simultaneous portal and hepatic arterial resection, and reconstruction. Resection lines for the hepatic artery, portal vein, and the left posterior sectional duct are shown by double lines.

FIGURE 90C.15 Intraoperative view after an extended left hepatic resection with total caudate lobectomy, extrahepatic bile duct resection, and portal vein resection and reconstruction. The vessel loop is around the right posterior sectoral artery. An autologous graft using the right external iliac vein is demonstrated. The right posterior superior (B7) and the right posterior inferior (B6) segmental bile ducts are divided separately above the reconstructed portal vein. RHV, right hepatic vein; RAHA, right anterior hepatic artery; A6, right posterior inferior segmental hepatic artery.

After confirmation of the course of the middle hepatic vein (MHV) using intraoperative ultrasonography, liver transection is performed along the demarcation line that appears after ligation of the right hepatic artery. On the caudal aspect of segment IV, the liver transection line is horizontally advanced approximately 1 cm ventral to the hilar plate to achieve a free surgical margin. When the MHV is exposed, liver transection is reduced toward the left, lateral to the distal portion of the ligamentum venosum. When the caudodorsal aspect of the MHV is completely exposed, the confluence of the MHV and IVC is seen. At this point, the caudate lobe can be turned and pulled ventrally from behind the left lateral segment. Finally, the bile duct is transected after placing a stay suture, and the right hepatic lobe is resected en bloc with the entire caudate lobe, portal bifurcation, and extrahepatic bile duct. The transected bile duct stumps, left medial sectional branch (segment IV), left lateral anterior sectional branch (segment III), and left lateral posterior sectional branch (segment II) are noted just to the right of the umbilical portion of the left portal vein (see Fig. 90C.7).

Bilioenteric continuity is reestablished using a Roux-en-Y jejunal loop. In our fashion, the jejunal limb is brought to the transected hepatic ducts via the retrocolic-antegastric or the retrocolic-retrogastric route (Nagino et al, 2002). We perform hepaticojejunostomy in one layer using a 5-0 absorbable monofilament suture; a biliary drainage tube is placed across all anastomoses either through the jejunal loop and/or transhepatically (Nagino et al, 2007).

Extended Left Hepatic Resection, Caudate Lobectomy, Extrahepatic Bile Duct Resection, and Portal Vein Resection and Reconstruction

Extended left hepatic resection with caudate lobectomy is used for hilar cholangiocarcinoma, which predominantly involves the left intrahepatic bile ducts in continuity with the duct to the right anterior section (see Chapters 50B and 90B). During the subhepatic dissection of the hepatoduodenal ligament, the left hepatic artery and middle hepatic artery, if present, are ligated and divided at their origins, and the right hepatic artery is carefully isolated up to its bifurcation into the anterior and posterior sectoral branches. Then the anterior sectoral branch and caudate lobe branches of the right hepatic artery are ligated and divided. Mobilization of the gallbladder provides a good operative view of the right posterior pedicle. The left portal vein is ligated and divided, followed by division of the right anterior branch of the right portal vein and caudate lobe branches arising from the main portal trunk and right portal vein. If cancer invasion of the portal bifurcation or the right portal vein is observed, combined portal vein resection and reconstruction is usually performed after liver transection for left hepatectomy or before liver transection in some cases of right hepatectomy. The caudate lobe and segment II and III are mobilized to the right, and the short retrohepatic caudate veins are ligated and divided, beginning on the left caudally and progressing cranially. When the confluence of the ligamentum venosum and the left hepatic vein (LHV) or IVC is displayed, the ligament is ligated and divided. The LHV and MHV are divided and closed with a running suture or a vascular stapler. The caudate lobe and the left lobe are then completely detached from the IVC.

Subsequently, the liver is transected along a demarcation line in the right portal scissura between the right anterior and right posterior sections. The course of the RHV is confirmed ultrasonographically. After parenchymal transection, the RHV should be exposed on the raw surface of the liver. The plane of the liver transection courses between the right posterior superior section (segment VII) and the right portion of the caudate lobe and begins from the sulcus on the right side of the caudate process and advances cranially along the right margin of the IVC. Finally, the right wall of the IVC is clearly exposed (Fig. 90C.16; see also Fig. 90C.15).

FIGURE 90C.16 Intraoperative image after extended left hepatic resection, caudate lobectomy, extrahepatic bile duct resection, and combined simultaneous resection of the right hepatic artery (RHA) and portal vein (PV). End-to-end anastomosis between the main PV and the right posterior sectional branch is accomplished (arrowhead). A posterior branch of the right hepatic artery (RHA post) and the proximal part of the RHA are cross-clamped with vascular clips. B6+7, stump of the right posterior sectoral bile duct; RHV, right hepatic vein.

The right posterior sectoral bile duct is exposed cranially to the right portal vein and is divided so as to obtain histologically free margins. Finally, vascular clamps are placed distally and proximally to the involved portal bifurcation: the distal clamp is placed obliquely to adjust the caliber of the distal portal vein to the transversely transected main portal trunk, and the specimen is resected en bloc, including the entire caudate lobe, the involved segment of the portal vein, and the extrahepatic bile duct. The portal vein reconstruction between the main portal trunk and the right posterior sectoral portal branch is then performed (see Fig. 90C.16), and an interposition graft of autogenous vein is often necessary (see Fig. 90C.15).

In some locally advanced cases, combined resection and reconstruction of the right hepatic artery with an end-to-end anastomosis is a requisite to achieve a negative margin (Fig. 90C.17; see also Fig. 90C.16). Microsurgical techniques are used for arterial reconstruction with or without using right gastroepiploic artery or radial artery as an interposition graft (Sakamoto et al, 2006). When arterial reconstruction is impossible, one potential countermeasure is creation of an arterioportal shunt to prevent possible leakage of the hepaticojejunostomy, liver abscess, and fatal liver failure (Kondo et al, 2004). Oblique-to-side anastomosis is performed between the common hepatic artery and the main portal vein. Three weeks after surgery, transcatheter arterial embolization of the common hepatic artery is carried out to prevent further portal hypertension. It must be remembered, however, that the development of liver failure or an abscess in the remnant liver are not eliminated by arterioportal shunting.

FIGURE 90C.17 Hepatic arterial reconstruction is through an end-to-end anastomosis between the proximal right hepatic artery and the posterior branch of the right hepatic artery with microscopic vascular techniques. The arrowhead shows the end-to-end anastomosis of the portal vein reconstruction. B6, stump of the right posterior inferior segmental bile duct; B7, stump of the right posterior superior segmental bile duct.