Surgical Management of Renal Cell Carcinoma (RCC) with Vena Cava Tumour Thrombus

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1 european urology supplements 5 (2006) available at journal homepage: Surgical Management of Renal Cell Carcinoma (RCC) with Vena Cava Tumour Thrombus Emanuele Belgrano a, Carlo Trombetta a, Salvatore Siracusano a, *, Giorgio Carmignani b, Giuseppe Martorana c, Giovanni Liguori a a Department of Urology, University of Trieste, Trieste, Italy b Luciano Giuliani Department of Urology, University of Genoa, Genoa, Italy c Department of Urology, University of Bologna, Bologna, Italy Article info Keywords: Renal cell carcinoma Thrombus Tumour invasion Vena cava involvement Abstract Objectives: Renal cell carcinoma (RCC) propagation into the inferior vena cava is rare (10 25%) and is described as an extension above the hepatic veins up to the right atrium or even into the right ventricle. Venous tumour invasion is associated with several prognostic factors such as local infiltration of perinephric tissue, lymph nodes metastases, caval infiltration, and the presence of distant metastases. We reviewed our experience with surgical treatment of RCC with vena cava involvement. Methods: We analysed the Urological Genoa School results from 1970 to 1985 on 28 consecutive cases (Giuliani s series) and between 1986 and 2005 on 59 of 81 cases from three Italian urologic academic centres (Trieste, Bologna, and Genoa). Results: For , the overall survival rate for all patients was 30% at follow-up periods of mo. With caval infiltration, the overall survival rate at 12 mo was 0%. For the period , the overall survival rate at 8 yr was about 80%. Nonsignificant differences for nodal stage and caval infiltration were observed during the two time periods. Conclusions: Our data confirm, as reported by others, that nonmetastatic RCC with extension into vena cava is potentially curable. # 2006 European Association of Urology. Published by Elsevier B.V. All rights reserved. * Corresponding author. Department of Urology, Cattinara Hospital, Via Strada di Fiume 447, Trieste, Italy. Tel ; Fax: address: siracus@univ.trieste.it (S. Siracusano). 1. Introduction Propagation of renal cell carcinoma (RCC) into the inferior vena cava (IVC) is rare, accounting for 4 10% of all renal carcinomas, with 10 25% of these patients presenting an extension above the hepatic vein up to the right atrium or even into the right ventricle [1,2]. Venous tumour invasion is associated with several prognostic factors such as local infiltration of perinephric tissue, lymph nodes metastases, caval infiltration and the presence of distant metastases [3]. As extensive tumour thrombi can be present without evidence of lymph node and distant /$ see front matter # 2006 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi: /j.eursup

2 european urology supplements 5 (2006) metastasis, an aggressive surgical approach with curative intent is justified [4]. Currently most authors agree that the presence of the thrombus itself has no specific prognostic significance if it can be removed successfully [5]. With advances in immunotherapy with such agents as interferon [6], control of distant metastases in patients with RCC extending into the IVC can be achieved; thus, survival of these patients may increase if aggressive surgery including tumour thrombectomy is combined with immunotherapy. It appears worthwhile to perform thrombectomy even in patients in whom RCC thrombus extends to the level of the right atrium or the pulmonary artery [7]. Meanwhile, there are several reports of larger series of patients who underwent radical surgery for RCC with IVC involvement, with 5-year survival rates of 32 64% [8 10]. In contrast, if only nephrectomy is performed, the prognosis is poor and almost all patients die within 1 year [11]. Several different surgical approaches have been described depending on the proximal extent of the tumour thrombus [4,12]. When the thrombus is localized within the infrahepatic IVC, tumour extraction usually is accomplished after proximal and distal control of the IVC. When the thrombus extends into the intrahepatic IVC or higher, exposure and isolation of the IVC are more extensive, requiring mobilization of the liver with or without the use of cardiopulmonary bypass (CPB) and, in some circumstances, must be accompanied by deep hypothermic circulatory arrest [13]. In this setting our purposes were to update the surgical treatment of RCC with vena cava tumour thrombus by focusing on the clinical series of the academic urologic centres of Trieste, Genoa and Bologna, and by comparing at the same time the results of two consecutive surgical experiences. segment of the vena cava (level III) and in the fourth into the atrium (level IV). The first strategic surgical step was to gain control over the vena cava portion above the thrombus by placing tourniquets or clamps to avoid an embolism during preparation of the tumour-bearing kidney Surgical technique In cases of level I and II tumours, laparotomy usually was performed through an anterolateral xipho-umbilical-subcostal approach, which is less invasive. If the thrombus was above the level of the hepatic veins, a cruciate Mercedes-like incision was carried out; in contrast, a median sternotomy was performed for level IV thrombus. Tumour excision started with cranial mobilization of the great omentum and the transverse colon; the ileum was then lateralized on the right, and an incision of the Treitz ligament and the posterior peritoneum was performed. The anteriorlateral surface of the aorta was identified. The renal vein, which crosses over the aorta, was identified and eventually retracted. The renal artery was then identified, carefully dissected up to its origin and ligated. A laterocolic incision and medial mobilization of the colon was then performed. The affected kidney was completely freed within Gerota s fascia en bloc with the adrenal gland by legation and section of the artery, ureter and vascular attachments, and was left attached only to the IVC. In case of left tumours, it was 2. Methods We report the results of the Urologic Genoa School from 1970 to 2005 on 109 consecutive cases. For convenience of analysis we reviewed the results between 1970 and 1985, and between 1986 and 2005, respectively. All RCCs were reassessed according to the 2002 TNM classification, Fuhrman s grade, caval infiltration, distant metastasis and tumour thrombus level propagation. According to the cephalad extension into the vena cava, the thrombus was classified into four categories [14] (Fig. 1). The first category encompassed patients with a tumour thrombus extending in the renal vein or for less than 2 cm into the infrahepatic segment of the IVC (level I). The second category included patients with a tumour thrombus extending into the IVC to below the hepatic vein (level II). In the third category the thrombus extended into the suprahepatic Fig. 1 Levels of inferior vena cava tumour thrombi.

3 612 european urology supplements 5 (2006) Level III thrombi In our experience patients with level III thrombi usually underwent surgical removal of the thrombus with the aid of venovenous bypass (VVB) without hypothermic circulatory arrest. The infrahepatic IVC was widely exposed by dividing the venous branches to the caudate and the left lobe of the liver, and legating the lumbar vessels. After dissection of ligaments, the liver was rotated downward, providing excellent exposure of the IVC, and a tape was placed around the hepatic hilum. Care was taken to isolate perforating veins, if present, to the caudate lobe; then they were ligated and divided. The diaphragm was exposed and incised in the midline, and the pericardium was opened. A tape was then placed around the intrapericardial IVC. The distal IVC and the inferior mesenteric vein were cannulated with a 20-F cannula and connected to the inflow side of a centrifugal pump (Bio-Medicus, Minnetouba, MN, USA). Pump outflow reached the right atrium through a short length of tubing with a heat exchanger and a 28-F venous cannula (Fig. 3). A reservoir was also branched to the venous side of the circuit to allow for rapid volume expansion. Patients were given a single bolus of 10,000 units of heparin. Vascular control was achieved by clamping the infrarenal and intrapericardial IVC, and the contralateral renal vessels. The hepatic artery and the portal vein also were clamped (Pringle manoeuvre) to lessen bleeding from the hepatic veins. VVB was established with flow in the range of 2 l/min, and the thrombus was removed safely en bloc with the kidney after a wide caval resection in a bloodless operating field. The vena Fig. 2 Tourniquet loops are placed around the inferior vena cava below the renal and hepatic veins and around the contralateral renal vein. transposed medially to the mesocolon. The vena cava was then dissected below the renal veins up to the level of the hepatic vein and the lumbar veins were clipped. Surgical options differed, depending on the cephalic extension Level I thrombi For level I thrombi, before the tumour-bearing kidney was mobilized, the infrahepatic portion of the IVC was completelyisolated,andasatinskyclampenclosingthethrombus was positioned on the IVC. This process allows en bloc resection of the renal tumour and the thrombus with a cuff of the vena cava Level II thrombi For level II thrombi, tourniquet loops were placed around the IVC below the renal and hepatic veins. The contralateral renal vein was occluded by a tourniquet (Fig. 2). The IVC was incised on the lateral side; the incision also extended over 2 cm of the ipsilateral renal vein. The thrombus was extracted after blunt dissection from the vessel wall. The caval wall incision was closed by a 4-0 polypropylene running suture. In one patient partial reconstruction with ovarian vein was necessary, because extensive partial phlebectomy narrowed the lumen of the IVC to less than 50% of its original diameter. Fig. 3 Diagram illustrating the venous bypass: Cannulae are placed into the right atrium, the distal inferior vena cava and the inferior mesenteric vein; in this manner venous blood from lower body and portal circle is delivered into the right atrium.

4 european urology supplements 5 (2006) Fig. 5 Life table of patients with caval thrombus who underwent radical nephrectomy. Fig. 4 Incision in the right atrium showing the presence of a free-floating thrombus. 3. Results 3.1. Surgical experience cava was closed with 4-0 polypropylene. The VVB was discontinued and the cannulae removed [15] Level IV thrombi For level IV tumours, CPB and hypothermic (20C) circulatory arrest was required. A cruciate Mercedes-like incision was made with a median sternotomy. Before complete mobilization of the tumour-bearing kidney, a retrohepatic portion of the IVC heparinization was performed, and the cannulae were placed into the aorta and right atrium. Cardiopulmonary bypass was then instituted with systemic cooling. Incision of the vena cava and removal of the retrohepatic portion of the thrombus were performed, followed by atriotomy and extraction of the atrial portion of the thrombus. After closure of the atriotomy and IVC, the patient was rewarmed. In one patient the thrombus extended from the IVC through the heart and into the pulmonary artery (Fig. 4). Cardiopulmonary bypass was achieved by means of the usual technique. The aorta was cross-clamped. Incisions in the right atrium and pulmonary artery revealed a free-floating thrombus, which was grasped through the right atrium and withdrawn intact. We reviewed the file records of 28 patients (median age, 68 years) (Giuliani s series) with a mean followup of 66 months. The stage of disease was pt3b in 22 of 28 (79.6%) patients, and pt3c in 6 of 28 (21.4%) patients, respectively. The percentage of survival at 12, 24, 48 and 60 months, in relation to level of caval thrombus, caval infiltration and distant metastases, are reported in Table 1, Figs. 5 and Surgical experience We reviewed file records from the departments of urology of Trieste, Bologna and Genoa of 59 of 81 (73%) patients (median age, 66 years) with a mean follow-up of 120 months. The stage of disease was pt3b and pt3c in 57 of 59 (97%) patients and in 2 of 59 (3%), respectively. The Fuhrman s grade was G2 in 19 patients (32%), G3 in 29 patients (49%) and G4 in 11 patients (19%). The tumour thrombus level, the nodal stage, the caval infiltration and the presence Table 1 Survival rate and median survival in patients with diagnosis of renal cell carcinoma with inferior vena cava thrombus in Giuliani s series No. of pts 12-month survival (%) 24-month survival (%) 48-month survival (%) 60-month survival (%) I 6 32 II III IV V 7 M0N All pts I = caval thrombus above hepatic veins; II = caval thrombus below hepatic veins; III = caval thrombus at renal veins level; IV = distant metastases; V = caval vein infiltration; M0N0 = caval thrombus alone (from La chirurgia del carcinoma renale Atlante by Luciano Giuliani, 1986); pts = patients.

5 614 european urology supplements 5 (2006) Fig. 6 Life table of patients with caval wall infiltration, distant metastases and caval thrombus alone (M0N0). of distant metastases are reported in Table 2. No perioperative mortality occurred in any case, while surgical morbidity attributable to pneumonia occurred in 6 of 59 (10.2%). Finally 10 of 59 (17%) of patients died within 72 months of the operation because of relapse of the disease. The statistical analysis was performed by Kaplan- Meier s test, allowing us to observe the following results: 1. The overall survival in all patients considering allcause mortality was 77.2% (Fig. 7). 2. The survival at 120 months in relation to thrombus level was 40 of 48 (83%) for level I subjects, 6 of 6 (100%) for level II, 2 of 3 (67%) for level III and 1 of 2 (50%) for level IV. 3. The survival at 120 months for nodal stage 0 was 78%, while the survival for involvement of one or more lymph nodes was not higher than 36 months (Fig. 8). Fig. 7 Kaplan-Meier cumulative estimates of overall 10- year survival rate. Table 2 Thrombus level, nodal stage, caval infiltration and presence of metastases in series Metastases [no. of cases (%)] No metastases Caval infiltration No caval infiltration Nodal stage 1 Nodal stage N0 Thrombus level pt3b (57/59) I: 48 (81.3) 45/57 (79.0) 12/57 (21.0) a 55/57 (96.5) 2/57 (3.5) b 50/57 (88.0) 7/57 (12.0) c II: 6 (10.1) III: 3 (5.1) pt3c (2/59) IV: 2 (3.4) 2/2 (100) 2/2 (100) 2/2 (100) Level I = 3 of 57 (5.0%) cases; level II = 6 of 57 (11.0%) cases; level III = 3 of 57 (5.0%) cases. b Level I = 0 cases; level II = 0 cases; level III = 2 of 57 (3.5%) cases. Level I = 0 cases; level II = 4 of 57 (7.0%) cases; level III = 3 of 57 (5.0%) cases. a c

6 european urology supplements 5 (2006) Fig. 8 Kaplan-Meier cumulative estimates of overall 10- year survival rate stratified by lymph nodes. 4. Death occurred within 12 months of the operation in more than 50% of patients with one or more positive lymph node (Fig. 9). 4. Discussion Renal cell carcinoma has a natural tendency to form tumour thrombus, which can propagate into the renal vein or the IVC [1 3]. This carcinoma invades the IVC in up to 10% of patients, involving the right atrium in 8% [16,17]. Radical excision of renal cancer with propagation into the IVC has become the accepted surgical approach since the mid-1970s when Marshall et al. and Skinner et al. [18,19] demonstrated that long-term survival could be achieved also in these patients. There has been much debate about the prognostic significance of cranial extension of the vena cava tumour thrombus. Currently most authors agree that the presence of the thrombus itself has no specific prognostic significance if it can be removed successfully [4,5,7 9]. With advances in immunotherapy with such agents as interferon alpha and interleukin 2 [6], control of distant metastases in patients with RCC extending into the IVC can be achieved. Moreover, new therapies such as tumour vaccines, anti-angiogenesis agents and small-molecule inhibitors are being developed to improve efficacy and to treat those patients who are unable to tolerate or are resistant to systemic immunotherapy [20]. Survival of these patients may increase if aggressive surgery including tumour thrombectomy is combined with immunotherapy. It appears worthwhile to perform thrombectomy even in patients in whom RCC thrombus extends to the level of the right atrium [7]. If aggressive surgical interventions and systemic therapies are combined, the prognosis of formerly untreatable patients can be improved dramatically. In patients with nonmetastatic RCC and IVC involvement, the 5-year survival rate ranges between 32% and 64% after complete surgical resection. In contrast, if only nephrectomy is performed, the prognosis is poor, and almost all patients die within a year [11]. Moreover the presence or absence of perinephric fat involvement, lymph node involvement or distant metastases are important prognostic factors. The presence of these adverse prognostic findings reduces survival [8,10,11,21,22]. The removal of a thrombus extending into the IVC without an adequate control can be the cause of two undesirable events: thrombus fragmentation with possible pulmonary embolism and uncontrollable haemorrhages attributable to lumbar, adrenal and suprahepatic veins bleeding [1,12,23] Laparoscopy Although laparoscopic surgery is being increasingly used for RCC confined to the kidney, there are only a few reports in the literature concerning tumours with thrombus in the renal vein treated laparoscopically; currently the gold standard therapy for caval thrombus is still open surgery [24 26] Imaging Fig. 9 Trend of deaths at 10-year follow-up. The extent of surgery depends on the level of IVC extension. Preoperative computed tomography (CT) was used initially to assess the primary tumour and

7 616 european urology supplements 5 (2006) other sites of potential disease. If IVC thrombus was seen by CT scan, Magnetic resonance imaging (MRI) was used to accurately delineate the level or extent of thrombus [27]. In the last years, we have not found vena cavography to be additive to CT scan and MRI. In four patients the preoperative investigations (CT scan, MRI and cavography) offered contradictory results regarding the exact cranial extension of the thrombus; therefore, an intraoperative ultrasound was performed to choose the most-suitable surgical approach. In our opinion intraoperative ultrasound provides excellent dynamic images of the thrombus and is definitive in ruling out the limits of the thrombus. We think that this technique should be encouraged in those patients in which the presence of renal vein or IVC involvement is dubious on the basis of preoperative imaging techniques [28] Embolization In three of our patients with extensive caval extension, we performed preoperative renal arteriography and renal artery embolization 24 to 72 h before the operation in an attempt to reduce tumour vascularity and to contract the tumour thrombus Surgical approach In case of big tumours or caval thrombus, we think the first surgical step is direct access to the renal artery at the level of the Treitz ligament [1,12]. The advantage of this manoeuvre is that it allows the control of the renal artery without any manipulation of the renal mass. Traditionally a thoracoabdominal incision was the approach of choice in these patients, but in the last few years surgeons discovered the advantages of a chevron incision [29] and the possibility of an abdominal transdiaphragmatic approach to the intrapericardial IVC when the thrombus is infradiaphragmatic [30]. The new approach allows earlier recovery and less pain, and eliminates the need for thoracic drains. Obviously if the tumour thrombus extends above the diaphragm, a midline sternotomy combined with an abdominal incision is mandatory. As a matter of fact, in our experience in cases of level I and II tumours, laparotomy usually was performed through an anterolateral xipho-umbilical-subcostal approach. If the thrombus was above the level of the hepatic veins, a cruciate Mercedes-like incision was carried out; sternotomy was performed for level IV thrombus [5,29]. Surgical strategy has changed radically according to the cephalic extension of the thrombus [1,12,5,29]. An infrahepatic thrombus (levels I and II) can be removed safely via a completely abdominal isolation of the IVC, clamping and cavotomy. On the other hand, in case of a thrombus extending to the right atrium, a large thoracoabdominal access with cardiocirculatory arrest is mandatory [31]. The surgical approach for level III caval thrombosis remains a debatable issue; as a matter of fact control of the suprahepatic or intrapericardial IVC is mandatory during removal of vena caval thrombi to prevent mobilization and minimize blood loss. Cardiopulmonary bypass with or without hypothermic circulatory arrest has been reported to manage level III thrombus, particularly when there is extension proximal to the major hepatic veins [29]. Although the usefulness of CPB in patients with level IV thrombus is obvious, its routine use in patients with level III thrombus is not mandatory, as shown by Parekh et al. and Ciancio et al. [32,33]. We think that perfect visualization of the suprahepatic and intrapericardial IVC can be achieved easily by an abdominal approach [30], and that the advantages of approaching the intrapericardial IVC through a limited diaphragmatic incision are that it is less invasive and avoids sternotomy. In addition, easy control of upper thrombus extension is achieved, and liver derotation and the difficult dissection of the IVC between the liver and the diaphragm are avoided. In contrast, some authors [34] recently have reported the use of liver transplant techniques of extensive liver mobilization to the left to facilitate exposure and control of the retrohepatic IVC, thus avoiding CPB and/or VVB. When cross clamping of the IVC is performed, it can lead to impaired venous return to the heart and consequently to central hypovolemic shock [15,35]. Moreover portal clamping leads to accumulation of toxic metabolites in the gut. Cardiopulmonary bypass with or without deep hypothermia and circulatory arrest has been used for radical nephrectomy with extended thrombectomy, but this technique is associated with significant perioperative morbidity and mortality [11]. As these techniques require full heparinization with possible significant bleeding problems, VVB has been employed as an alternative to full bypass when thrombus growth remains below the level of the suprahepatic veins. In our experience pump-driven VVB is another safe and useful procedure in the management of RCC with caval involvement below the suprahepatic veins, and avoids the important risks related to cardiac arrest, allowing normal perfusion of vital organs. Portal decompression is performed by cannulation of the inferior mesenteric vein and avoids the accumulation of toxic products

8 european urology supplements 5 (2006) in the gut. This technique does not require full heparinization. We think that CPB should be reserved for those patients with level IV thrombi in whom adequate visualization for thrombectomy cannot be achieved otherwise. When the tumour thrombus invades the IVC wall, partial or total circumferential resection of the IVC with adequate surgical margin is necessary. However, the indication and method of venous reconstruction after resection of the suprarenal IVC are not yet established. After resection, graft angioplasty is not mandatory in all patients and remains a controversial issue. However, possible adverse consequences of the absence of venous reconstruction are venous insufficiency of the lower limbs and renal failure. Thrombosis may occur if the lumen of the vena cava is reduced to less than 50% of its normal diameter. Graft replacement of the IVC is an easy and safe procedure leading to good functional results. Alloplastic materials such as Dacron and Gore-Tex can be used, but autologous materials have a lower thrombosis rate [36] and a greater resistance to infection in the lower flow venous system than prosthetic material. The saphenous vein might be considered, but its use requires another uneconomical incision. Partial resection of the IVC followed by patch-angioplasty with pericardium also has been reported [36]. The ovarian vein is another possibility: It is available in the same operating field, because it is removed during the procedure and can be used safely, because it is placed outside the neoplastic area [37]. It is well-known that, in patients with nonmetastatic RCC and IVC involvement, the 5-year survival rate ranges between 32% and 64% after complete surgical resection [8 10]. The presence or absence of perinephric fat involvement, lymph node involvement or distant metastases represent adverse prognostic findings. Nevertheless at present there is a controversy concerning the prognostic significance of the tumour thrombus level in IVC [11,38 39]. After analyzing our results and comparing the two periods of surgical experiences, we believe that it is useful to comment on some considerations of survival in relation to prognostic factors as previously reported. In the first period (Giuliani s series) the overall survival is comparable with the data reported in the literature. This aspect seems to differ when we analyze the overall survival of patients belonging to the surgical experience ranging from 1986 to In fact in this series the overall survival at 8 years follow-up is approximately 80%. This substantial difference could be justified by probable different biologic behaviour of the tumour under the same stage of disease and by the improvement in preoperative selection and postoperative care of these patients. On the contrary we observed nonsignificant differences from the two periods of analysis regarding the survival in relation to the nodal stage and the caval infiltration. Finally a particular consideration is needed when we analyze survival results in relation to the thrombus level in IVC. The overall analysis of the two series together shows a significant correlation between survival and IVC thrombus level. Nevertheless this aspect is not completely agreed upon, as reported by others. In fact Sosa et al. [11] described a 2-year survival rate of 80% in patients with infrahepatic IVC tumour thrombi, compared with only 21% in those with suprahepatic thrombi. They found that patients with suprahepatic caval extension were more likely to have perinephric fat and regional lymph node involvement [11]. On the contrary Skinner et al. [8] reported a 5-year survival rate of 35% after surgical treatment for patients with RCC and infrahepatic IVC thrombus, 18% for those with intrahepatic IVC thrombus and 0% for those with atrial tumour thrombi. 5. Conclusion Although these data are limited because of the small number of patients, our long-term experience confirms that nonmetastatic RCC with extension into the IVC potentially is curable and that the surgical techniques currently used for the removal of the tumour thrombus are justified. References [1] Giuliani L, Giberti C, Martorana G, Rovida S. Radical extensive surgery for renal cell carcinoma: long-term results and prognostic factors. J Urol 1990;143: [2] Ljungberg B, Stenling R, Osterdahl B, Farrelly E, Aberg T, Roos G. Vein invasion in renal cell carcinoma: impact on metastatic behavior and survival. J Urol 1995;154: [3] Novick AC, Campbell SC. Renal tumors. 8th ed Walsh PC, Retik AB, Vaughan ED, Wein AJ, editors. Campbell s urology, vol 4. 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