Complete Obstruction of the Inferior Vena Cava

When liver tumor is associated with complete inferior vena cava (IVC) obstruction, collateral circulation usually provides sufficient venous drainage (Fig. 91B.1), therefore obstruction symptoms, such as edema of the lower extremity, are uncommon. Leiomyosarcoma of the retrohepatic IVC is the main etiology of a complete obstruction of the IVC. In this situation, liver resection with concomitant IVC resection is appropriate, providing preservation of the collaterals can be performed without restoration of caval flow. IVC replacement is considered in patients who have poor development of collateral circulation and in those who require wide retroperitoneal resection for lymph node dissection, which can disrupt preexisting venous channels and reduce collateral venous return (Beck & Lalka, 1998; Yoshidome et al, 2005).

FIGURE 91B.1 Complete obstruction of the inferior vena cava with development of collateral circulation.

After IVC resection, lower-limb venous thrombosis occurs in about 25% of patients, and reduction of the collateral circulation may increase this risk (Mingoli et al, 1991). After caval flow interruption, postoperative renal dysfunction occurs in 0% to 40% (Daylami et al, 2010). Because the left renal vein has multiple collateral venous developments—gonadal, adrenal, and lumbar—ligation of the left renal vein is not deleterious (Griffin & Sterchi, 1987); however, the right renal vein has few collateral venous systems, and its ligation can be harmful and often necessitates reimplantation into the IVC or into the left renal vein.

Partial Obstruction of the Inferior Vena Cava

Colorectal liver metastasis and intrahepatic cholangiocarcinoma (see Chapters 50A and 81A), which are best treated by R0 resection, may involve the IVC. Preoperative morphologic assessments are generally inaccurate to differentiate malignant infiltration of the vena cava wall from a simple tumoral adhesion; therefore concomitant hepatic and IVC/HV resection should be considered when tumor involvement of the IVC or the venous confluence is suspected. Invasion of the vena wall is found in 22% to 72% of patients and can be assessed intraoperatively by palpation, ultrasonography, or even by intravascular ultrasonography (Azoulay et al, 2006; Hemming et al, 2002; Kaneko et al, 1996; Kikumori et al, 2003). Experience in living donor liver transplantation (LDLT) has shown that congestion of the remnant liver territory is underestimated (Scatton et al, 2008). Impairment of venous outflow of the remnant liver has deleterious consequences on postoperative liver function and regeneration, emphasizing the need for reconstruction of the corresponding draining HV, especially when the volume of the remnant liver is marginal (Nakamura et al, 1990). In addition, maintaining the normal anatomy of the hepatic veins in the remnant liver may be beneficial to preserve the possibility of repeat hepatectomy for tumor recurrence, particularly in patients resected for colorectal liver metastasis (Pessaux et al, 2006).

Many studies report the technical aspects of vascular resection with hepatectomy, but few report the long-term results with survival rate. Venous involvement is a poor prognostic factor, but given the poor results of nonsurgical treatment, aggressive surgical resection that includes major vascular resection offers the best results in selected patients (Aoki et al, 2004; Miyazaki et al, 1999).

Hepatocellular carcinoma (HCC) has a strong propensity for vascular invasion and direct intravascular extension (see Chapter 80). Autopsy series report IVC involvement from 9% to 26% and right atrium involvement from 2.4% to 6.3% (Sung et al, 2008). Most patients are seen initially with symptoms of portal hypertension or right-sided heart failure (diuretic-resistant lower extremity edema). Efficient treatment requires liver parenchymal resection associated with vascular resection and thrombectomy under vascular exclusion (see Chapter 91A). This procedure, which requires expertise in both vascular and liver surgery, usually includes simultaneous hepatectomy and thrombectomy under vascular exclusion (Sung et al, 2008). Major bleeding and difficult vascular reconstruction are associated with the risk of thrombus migration into pulmonary arteries (Shirabe et al, 2001). When tumor thrombus extends to the right atrium, liver resection associated with cardiopulmonary bypass should be considered.

Resection

According to the extent and location of the IVC involvement, various approaches, including thoracoabdominal access, have been described (Torzilli et al, 2007). Because complete mobilization of the liver could be hazardous, an anterior approach to the IVC can be performed (Liu et al, 2000). After extrahepatic control of the IVC below and in the upper liver, the anterior approach includes initial liver resection toward the IVC.

If the portion of the IVC involved by the tumor is below the hepatic veins, the hepatic parenchyma is divided using intermittent inflow occlusion if necessary (Belghiti et al, 1999). Once the IVC is exposed, portal inflow occlusion is released if used, the patient is volume loaded, and clamps are placed above and below the area of tumor involvement (Fig. 91B.2; see Chapter 91A). This caval clamping allows resection of the portion of the liver involved by tumor with the portion of vena cava involved by tumor, followed by partial or total reconstruction of the IVC. Positioning the clamps below the hepatic veins allows perfusion of the remnant liver and minimizes ischemic time.

FIGURE 91B.2 Clamps placed above and below the area of tumor involvement on the inferior vena cava.

In cases of lateral IVC involvement, a single clamp may be applied tangentially to the IVC to preserve a vena caval flow (Fig. 91B.3), but this procedure is not applicable when the tumor involves the whole hepatocaval confluence. In such cases, are two different approaches may be applied. The first one includes a total vascular exclusion of the liver with subsequent infrahepatic IVC, pedicular, and suprahepatic IVC clamping (Fig. 91B.4; see Chapter 91A). Total vascular exclusion induces a decrease of 40% to 50% in the cardiac index and may be not well tolerated in some patients (Azoulay et al, 2006; Hemming et al, 2004). The second one includes use of an active venovenous bypass between the portal and axillary vein and between IVC and axillary vein can also be used (Azoulay et al, 2006; Hemming et al, 2004). When a biopump is used, in situ hypothermic perfusion of the liver parenchyma can be added to prevent postoperative liver failure as a result of prolonged ischemia (Azoulay et al, 2006; Hemming et al, 2004; see Chapter 94).

FIGURE 91B.3 A single clamp could be applied tangentially to the inferior vena cava to preserve vena caval flow in case of lateral wall involvement.

FIGURE 91B.4 Total vascular exclusion of the liver: the infrahepatic vena cava, hilum, and suprahepatic vena cava are serially clamped.

Extrahepatic control of the IVC can be attained without using total hepatic vascular exclusion (Varma et al, 2007). The suprahepatic IVC is taped just below the diaphragm, the common trunk of the left and middle hepatic veins is dissected, and a previously deployed suprahepatic tape is rotated to the right side between the vena cava and common trunk; this isolates the right hepatocaval confluence and juxtahepatic vena cava, leaving the common trunk and the rest of IVC free. The infrahepatic IVC is clamped, and concerning the suprahepatic IVC, a clamp is placed obliquely to occlude the right hepatocaval confluence and juxtahepatic vena cava (Fig. 91B.5). When right the hepatocaval junction is uninvolved, this procedure can be used in patients with left-sided neoplasms by reversing the caval tape to the left side (Maeba et al, 2001). The remnant liver receives complete inflow with uninterrupted outflow through the uninvolved hepatocaval confluence, the patency of which is maintained. This technique may also be used when synchronous involvement of the IVC and any one of the hepatocaval confluences is apparent, with at least one HV being free of tumor. This procedure has the potential disadvantage of incomplete vascular control during parenchymal transection in the presence of large veins from the caudate lobe, which leads to backflow venous bleeding. This problem can be overcome by associated resection of segment I.

FIGURE 91B.5 The infrahepatic vena cava is clamped, and a clamp is placed obliquely on the suprahepatic inferior vena cava to occlude right hepatocaval confluence and juxtahepatic vena cava.

Advances in liver transplantation techniques have allowed expansion of the ex vivo procedure in selected resections (see Chapter 94). This challenging technical procedure, described by Pichlmayr and colleagues (1988), is seldom performed (Hemming & Cattrall, 1999; Miyazaki et al, 2007b; Yanaga et al, 1993). Although a biopump ensures venous return to the supradiaphragmatic venous system, the liver is completely removed and perfused with preservation solution. Bloodless transection of hepatic parenchyma can then be performed, allowing complex reconstruction of hepatic veins or portal structures before reimplantation of the liver. A simplified technique was proposed with preservation of the continuity of the portal triad (Sauvanet et al, 1994). This technical modification reduces the duration of the anhepatic phase and avoids the risks of artery and biliary reconstruction.

Reconstruction

Hepatic Vein

Autologous vein graft using the external iliac, superficial femoral, saphenous, ovarian, portal, and left renal vein has been used for hepatic vein reconstruction (Nakamura et al, 1990, 1993; Ohwada et al, 1998; Takayama et al, 1996). The quality of the anastomosis itself and the blood flow volume through the graft are a concern in the long-term patency after a hepatic vein reconstruction. The selection of an optimal graft size is also important. Hepatic reconstruction using autologous vein grafts obtained from the upper abdominal cavity could be performed without requiring an additional skin incision. In addition, the portal vein or uninvolved hepatic vein from the resected specimen could be used (Hemming & Cattral, 1999), provided it is not involved with tumor; however, it has been reported that interposition grafts are complicated by thromboses in about 25% of patients (Nakamura et al, 1993). Venous graft must be kept as short as possible to avoid kinking, a risk factor for occurrence of thrombosis; however, grafts are not always necessary (Hemming et al, 2002; Nakamura et al, 1997). Even if cut flush with the liver surface, an HV can be anastomosed without an extension graft to either the origin of the same HV or, if necessary, lower down on the IVC. It is necessary to fashion a long, isolated segment of the HV (Oshita et al, 2009).

The advantage of expanded polytetrafluoroethylene (ePTFE) graft is the range of lengths and diameters that can be easily obtained (Fig. 91B.6). Potential disadvantages include long-term stricture and thrombosis. A synthetic graft carries a high risk of infection in cases of hepatic resection, especially with concomitant bilioenteric anastomosis or in cases with high risk of postoperative bile leakage, such as after segment VIII resection or after a resection close to the portal bifurcation (Yamashita et al, 2001).

FIGURE 91B.6 Central hepatectomy with resection of the right hepatic vein reconstructed by extended polytetrafluoroethylene graft.

Complete Obstruction

The complete obstruction of the portal vein with cavernous transformation remains a contraindication for the resection. In cases of HCC involving portal veins, the liver Cancer Study Group of Japan classifies the tumor invasion of the first branch of the portal vein and tumor in the main portal trunk or the opposite-side portal branch into two groups, vp3 and vp4 (Liver Cancer Study Group of Japan, 2003), because there might be a crucial difference between both groups in terms of therapeutic and prognostic aspects. Tumor thrombus of vp3 can be completely removed by a major hepatectomy with the division of the ipsilateral portal branch near the bifurcation, but vp4 tumor thrombus must be removed by a thrombectomy or via an en bloc combined resection and reconstruction of the main portal vein with the hepatectomy.

The difference in outcome between thrombectomy and partial portal vein resection is clear: Konishi and colleagues (2001) reported a 2-year survival rate of 34% with a 0% postoperative mortality rate following thrombectomy. Wu and colleagues (2000) reported a 2-year survival rate of 48% with 0% postoperative mortality following hepatectomy with combined partial portal vein resection. These results were confirmed by Inoue and colleagues (2009), who reported no survival difference in patients with macroscopic portal tumor thrombus undergoing a thrombectomy and a portal vein resection. Tumor thrombus derived from HCC grows expansively and rarely infiltrates the portal wall. It is logical to assume that if the tumor thrombus does not infiltrate into the portal venous wall, thrombectomy is a viable treatment option.

Partial Obstruction

Hilar or intrahepatic cholangiocarcinoma and liver metastases could involve the portal bifurcation (see Chapter 50A, Chapter 50B, Chapter 50C, Chapter 50D ). An en bloc portal vein resection may be necessary to achieve local tumor clearance and to increase resectability. In cases of hilar cholangiocarcinoma, infiltration or perivascular involvement after portal vein resections are present only in 22% and 13%, respectively (Neuhaus et al, 1999). No-touch techniques are generally used in oncologic surgery to prevent dissemination of tumor cells. Right-sided liver resections follow this principle, all the more so if the resection line is extended to the left portion of the hepatoduodenal ligament by portal vein resection. It is unnecessary to strip the right portal vein branch of the hepatic duct bifurcation, and the portal bifurcation can be left undisturbed as well, which further decreases the required extent of hepatoduodenal dissection. Recent studies have reported improved postoperative outcomes similar to those in patients without portal vein resection with a mortality rate of less than 10% (Bachelier et al, 2011; Kondo et al, 2003; Miyazaki et al, 2007a; Neuhaus et al, 1999). Neuhaus and colleagues (1999) reported a 5-year survival rate of 65% for patients who underwent hepatectomy with en bloc portal vein resection.

Resection (See Chapters 50B and 90B)

After completion of a lymphadenectomy down to the celiac trunk, the common bile duct and the portal trunk are dissected and encircled by a loop just above the pancreas. The right hepatic artery generally crosses behind the tumor and is isolated close to the proper hepatic artery. The left hepatic artery courses some distance to the tumor and is isolated up to the umbilical fissure. The bile duct is divided at the superior margin of the pancreas, and the right hepatic artery is divided. The proper and left hepatic arteries are fully isolated from the tumor region. The only connections of the hepatic hilum with the tumor to the surrounding structures are the main portal vein trunk and the left portal vein branch. Parenchymal transection is then performed. In case of bleeding during liver transaction, the hepatic pedicle is occluded by intermittent clamping (10 minutes clamping, 5 minutes clamping release). The specimen is attached to the portal vein bifurcation only; both parts of the portal vein are occluded with vascular clamps, superior to the duodenal bulb and within the umbilical fissure, respectively. Portal vein reconstruction is performed under portal vein occlusion only, in order to preserve the arterial hepatic flow.

Some authors have reported portal vein resection and reconstruction before hepatic dissection (Kondo et al, 2003). The risk of this technique is that surgical maneuvers after portal vein reconstruction might produce tension on the portal anastomosis, leading to its disruption.

Reconstruction

In most portal vein resections, end-to-end reconstruction can be performed without using segmental grafts. A continuous suture should be used, and an oblique cut on the left portal vein branch is performed to allow for the difference in caliber of the two ends. To avoid stricture, the surgeon should carefully reconstruct the portal vein without kinking in the reconstruction portion. This is achieved by maintaining precise anterior-posterior orientation when placing vascular clamps. Sufficient expansion of the reconstructed vein should be obtained by release of a proximal vascular clamp before the suture is tied, which should be done relatively loosely to allow for expansion. The right colon and the root of the mesentery are mobilized to obtain enough length to perform a tension-free anastomosis. In the literature, autologous vein grafts have been reported, such as external and internal iliac, jugular, or left renal veins.

Indication

Hilar cholangiocarcinoma and advanced gallbladder cancer (see Chapters 49 and 50B) have the propensity to invade extensively, not only along the bile duct but also into adjacent organs via lymphatics and perineural spaces. Regions of the portal vein and right hepatic artery bifurcations are often involved, because these vessels run just behind the bile duct and to the left of the gallbladder neck. Hepatic artery resection is less common, because the reconstruction is more complicated, and microvascular techniques are required. Furthermore, this level of invasion is often associated with advanced disease that is not amenable to resection, particularly in cases of gallbladder cancer; however, hepatectomy with combined portal vein/hepatic artery resection and reconstruction has been reported (Miyazaki et al, 2007a; Shimada et al, 2003). Hepatic artery resection may result in a higher postoperative mortality rate than portal vein resection, because hepatic artery resection has been combined with portal vein resection in most patients: the mortality rate could reach 33% to 56% (Gerhards et al, 2000; Miyazaki et al, 2007a, 2007b).

The survival rate is very poor after hepatic artery resection. Miyazaki and colleagues (2007b) reported 1- and 3-year survival rates of 11% and 0%, respectively, similar to unresectable patients, with survival rates of 15% and 0% at 1 and 2 years. A surgical team reported controversial results, with acceptable mortality, by an experienced surgeon (2%) and acceptable long-term survival in selected patients (30.3% at 5 years) (Nagino et al, 2010). The authors explained these good results by the fact that arterial vascular reconstruction was performed by plastic or vascular surgeons under a surgical microscope, they had previous experience with portal resection, and they practiced meticulous perioperative management.

Resection

To avoid long-term ischemic liver injury during both the resection and reconstruction of the hepatic artery and the portal vein, simultaneous resection and interruption of both vessels should be avoided. The portal vein should be resected first and reconstructed prior to hepatic artery resection. Then immediately after the reconstruction of the portal vein, the hepatic artery can be resected with the surgical specimen.

Reconstruction

The hepatic artery can be reconstructed in an end-to-end fashion in most patients, and the use of the gastroduodenal artery has been reported as a conduit. The anastomosis may be difficult or impossible to perform, when the arterial stump is small or when there are multiple vessels. Experimental studies using dogs subjected to hepatobiliary dearterialization demonstrated that arterioportal shunting reduced acute hypoxic hepatic injury and improved hypoxia in the bile duct, permitting successful choledochojejunostomy (Munemura, 1995), enhancing hepatic regeneration, and resulting in improved survival (Shimizu et al, 2000). In the literature, few clinical cases report the feasibility and safety of arterioportal shunting as an alternative procedure (Kondo et al, 2004; Young et al, 2008). Hepatopetal arterial collaterals develop within 1 month, and the shunt could be closed when still patent to prevent portal hypertension (Kondo et al, 2004).