Renal cell carcinoma with extension of tumor thrombus into the vena cava: Surgical strategy and prognosis

Renal cell carcinoma with extension of tumor thrombus into the vena cava: Surgical strategy and prognosis Yoshihiko Tsuji, MD, a Akinobu Goto, MD, b Isao Hara, MD, b Keiji Ataka, MD, a Chojiro Yamashita, MD, a Yutaka Okita, MD, a and Sadao Kamidono, MD, b Kobe, Japan Purpose: The outcome of patients who underwent radical resection of renal cell carcinoma extending into the vena cava was retrospectively analyzed, and risk factors for long-term survival were investigated. Methods: From 1983 to 1999, 33 patients who had renal cell carcinoma with inferior vena caval tumor extension underwent 34 surgical procedures. There were 27 men and six women with an average age of 60.1 years. Twenty-two cases (64.7%) were classified as stage III (T1-2 N1 M0 or T3 N0-1 M0), and 12 cases (35.3%) as stage IV (T4 or N2-3 or M1). Coexistent lung metastasis was found in seven cases (20.6%). The tumor thrombi invaded into the inferior vena cava below the hepatic hilum in 19 cases, below the orifice of hepatic veins in 12, and above the diaphragm in 3. Cardiopulmonary bypass graft was applied in 13 cases (38.2%). Inferior vena cava was reconstructed by direct suture (n = 19), polytetrafluoroethylene patch angioplasty (n = 13), or graft replacement (n = 2). Results: Two patients died during the early postoperative period because of retrohepatic caval injury and intraoperative pulmonary embolism. Late death occurred in 16 patients; the causes of death were tumor recurrence in 15 and acute pulmonary embolism as a result of graft thrombosis in 1. Overall 1-, 5-, and 10-year survival rates were 70%, 44%, and 26.4%, respectively. One- and 5-year survival rates were 81.3% and 52.9% for stage III and 50% and 31.2% for stage IV; a statistically significant correlation was found between surgical staging and survival (P =.049). Patients without lymph node metastasis had a significant survival advantage over those with lymph node metastasis (P =.022). There was no significant difference in survival on the basis of the presence or absence of synchronous lung metastasis (P =.291). The degree of local extension of the tumor or the level of tumor thrombus did not tend to influence survival. Conclusions: Surgical prognosis in patients with renal cell carcinoma extending into the vena cava was determined by the staging of the tumor, especially lymph node status, and not by the level of tumor thrombus or the presence of concurrent lung metastasis. The use of cardiopulmonary bypass graft is recommended for the resection of tumor thrombus extending over the diaphragm. (J Vasc Surg 2001;33:789-96.) Tumor thrombus extended into the inferior vena cava (IVC) is occasionally found in the advanced stage of malignant neoplasms, such as retroperitoneal tumors, gynecologic tumors, hepatocellular carcinoma, and renal cell carcinoma (RCC). 1-4 RCC, which has a tendency for vascular invasion, extends into the IVC in 4% to 25% of all patients. 5-8 In patients with nonmetastatic RCC who underwent radical nephrectomy and complete thrombectomy, 5-year survival rates of 30% to 72% have been reported. 9-11 However, surgical indication for patients with metastatic RCC and the use of cardiopulmonary bypass (CPB) during vena caval thrombectomy are still controversial. Prognosis-limiting factors of patients who underwent radical nephrectomy and complete thrombectomy are also uncertain. In this study we retrospectively analyzed the surgical outcome of patients who had RCC with IVC tumor thrombi. From the Departments of Surgery, Division II, a and Urology, b Kobe University School of Medicine. Competition of interest: nil. Reprint requests: Y. Tsuji, MD, Department of Surgery, Division II, Kobe University School of Medicine, 7-5-2, Kusunoki-Cho, Chuo-Ku, Kobe 650-0017, Japan. Copyright 2001 by The Society for Vascular Surgery and The American Association for Vascular Surgery. 0741-5214/2001/$35.00 + 0 24/1/111996 doi:10.1067/mva.2001.111996 PATIENTS AND METHODS Between January 1983 and December 1999, 33 patients who had RCC associated with IVC tumor thrombus underwent 34 surgical procedures. The 27 men and six women had an average age of 60.1 years, ranging from 34 to 79 years. RCC involved the right and left kidneys in 30 and three patients, respectively. One patient had redo operation for recurrent IVC tumor thrombus 2 years after his radical nephrectomy and complete vena caval thrombectomy. All of the 33 patients presented with symptoms for RCC; 28 had hematuria and 23 had abdominal or flank pain. Bilateral leg edema due to IVC obstruction was found in eight patients (24.2%). No patients presented with evidence of hepatic vein obstruction, such as ascites or hematemesis from esophageal varices. All patients preoperatively underwent routine blood tests, chest radiography, and renal arteriography to evaluate the tumor vascularity. Computed tomography (CT) and magnetic resonance imaging (MRI) of the abdomen were also performed to assess the existence of tumor thrombus, gross lymph node involvement, and metastatic disease. The level of tumor extension into the IVC could be exactly estimated by contrast enhanced CT and sagittal view of MRI. A bone scan, venacavography, chest CT, and/or brain CT were also obtained in some patients. 789

790 Tsuji et al April 2001 Table I. TNM staging of renal cell carcinoma with IVC tumor thrombus Stage T N M No. of cases III 3b 0 0 19 3b 1 0 2 3c 0 0 1 Total 22 IV 3b 0 1 5 3b 1 1 1 3b 2 0 1 3b 2 1 1 3c 2 0 2 4 0 0 2 Total 12 T3, tumor with perinephric invasion within Gerota s fascia; T3b, tumor with venous invasion extended to the infradiaphragmatic IVC; T3c, tumor with venous invasion extended to the supradiaphragmatic IVC; T4, tumor with perinephric invasion extended over Gerota s fascia. N0, no lymph node metastasis; N1, one metastatic lymph node of 2 cm or less; N2, some metastatic lymph nodes of 5 cm or less; N3, some metastatic lymph nodes greater than 5 cm. M0, no distant metastasis; M1, with distant metastasis. Staging system. Surgical staging was done according to TNM classification (TNM Atlas, third edition, 2nd revision, 1992) of UICC (Union Internationale Contre le Cancer). Twenty-two cases (64.7%) were classified as stage III (T1-2 N1 M0 or T3 N0-1 M0) and 12 cases (35.3%) as stage IV (T4, N2-3, or M1) (Table I). Concurrent distant metastasis was recognized in seven cases (20.6%), and all of them were lung metastasis. The extension levels of tumor thrombi were defined by three categories: Va, below the hepatic hilum (n = 19); Vb, below the junction of hepatic veins (n = 12); and Vc, above the diaphragm (n = 3) (Fig 1). Patients with tumor thrombus localized within the renal vein were excluded from this study. Surgical procedures. The operative techniques changed during this time period. In the first several cases, CPB was used in all cases. Surgical experience clarified that the total clamp of IVC below the orifice of hepatic veins without CPB did not induce hypotension or intestinal congestion; thus recently CPB has been applied only in cases of level Vc tumor. Present surgical details are as follows. In supine position, transesophageal echocardiography (TEE) probe was inserted after endotracheal intubation. With the use of intraoperative TEE, vascular clamp could be made exactly above the head of tumor thrombus, intraoperative pulmonary embolism could be diagnosed immediately, and the residual tumor thrombus into the IVC could be observed. Median laparotomy was used, and the IVC and the renal veins were exposed. In the case of level Va tumor, the vascular isolations were made on the IVC below the hepatic hilum, the infrarenal IVC, and the contralateral renal vein. The tumor thrombus was then removed through the longitudinal cavotomy incised from the level of the head of tumor thrombus to the orifice of renal vein. For level Vb tumor, an additional right subcostal incision was occasionally required to expose the retrohepatic IVC with mobilization of the right hepatic lobe. The vascular isolations of the IVC below the orifice of hepatic veins, the infrarenal IVC, and the contralateral renal vein were made without CPB, and the tumor thrombus was removed through the longitudinal cavotomy incised from the level of the head of tumor thrombus to the orifice of renal vein. In the case of level Vc tumor, an additional median sternotomy was performed, and the IVC below the cavoatrial junction was isolated. After heparinization, the femoral artery and vein were cannulated and normothermic partial CPB was started. The vascular isolations of the IVC below the cavoatrial junction, the infrarenal IVC, and the contralateral renal vein were made. The tumor thrombus was removed through the longitudinal cavotomy, while bleeding from the hepatic veins was sucked and returned in the CPB circulation. A Pringle maneuver was occasionally used to reduce the bleeding from hepatic veins. Suture closure or patch angioplasty was started from the proximal end, and CPB was weaned after closure of hepatic portion of the IVC. When the tumor thrombus extended into the right atrium, secondary venous cannula was placed in the superior vena cava. Then the tumor was removed through a right atriotomy under total CPB and electrically induced ventricular fibrillation. No systemic cooling or cardiac arrest was necessary. When the wall of the IVC was invaded by the tumor, the infiltrated portion was resected with an appropriate surgical margin. Depending on the defect size, the IVC was closed directly or reconstructed by polytetrafluoroethylene (PTFE) patch angioplasty or PTFE graft replacement. Follow-up and statistical methods. Patients, if their physiologic conditions permitted, received postoperative immunotherapy with interferon. All surviving patients were contacted at the time of data collection to determine disease status. Mean follow-up period was 31 months, ranging from 1 to 136 months. Survival time was calculated from the date of operation to date of death or last contact. Survival curves were calculated with the Kaplan-Meier method. Statistical difference between survival of subgroups was tested with the log-rank test, in case propriety of rank test was verified by the comparison of each cumulative hazard curve. RESULTS Intraoperative findings. Radical nephrectomy with tumor thrombectomy was performed in all patients. The IVC occluded by the tumor thrombus was generally enlarged, and the average diameter was 40.1 mm (range, 30-50 mm). Surgical approaches used were median laparotomy in 20 cases, median laparotomy with right subcostal incision in 5, and with sternotomy in 9 (Table II). CPB was used in 13 cases (38.2%), and mean CPB time was 50.7 minutes (range, 35-75 minutes). The IVC reconstructions were performed with direct closure in 19 cases, PTFE patch angioplasty in 13, and PTFE graft replacement in 2. Mean operative time was 405 minutes (range, 185-655 minutes), and the average blood loss was 2.5 L (range, 0.3-12 L). When categorized by surgical stage, 21 patients had stage III disease, and 12 had stage IV. Operative results. Two operation-related deaths were encountered. A male patient with a level Vb tumor throm-

Volume 33, Number 4 Tsuji et al 791 Fig 1. Classification of extension level of tumor thrombus into IVC: Va, tumor thrombus below hepatic hilum; Vb, tumor thrombus below orifice of hepatic veins; Vc, tumor thrombus above diaphragm. RK, Right kidney; LK, left kidney; RHV, right hepatic vein; MHV, middle hepatic vein; LHV, left hepatic vein; IVC, inferior vena cava. Table II. Surgical approach and the use of CPB Level of tumor thrombus Surgical approach n With CPB Va (n = 19) Median laparotomy 17 0 Median laparotomy with sternotomy 2 2 Vb (n = 12) Median laparotomy 3 1 Median laparotomy with right subcostal incision 5 3 Median laparotomy with sternotomy 4 4 Vc (n = 3) Median laparotomy with sternotomy 3 3 Total 34 13 bus underwent thrombectomy through the incision made on infrahepatic IVC. The retrohepatic IVC was accidentally torn during the procedure because the tumor thrombus was firmly invaded to the IVC wall. He died 15 days after operation of multiple organ failure induced by massive bleeding. The other patient was a man with a level Vb tumor thrombus. Sudden hypotension because of acute pulmonary embolism occurred during dissection around the right kidney. Emergency pulmonary thrombectomy was attempted under CPB; however, he died 1 day later of acute heart failure. The other 31 patients had no fatal complications, such as hepatic or renal failure, during their hospital stay. Prognosis and long-term survival. Sixteen (51.6%) of 31 early survivors died during follow-up. A woman who underwent IVC reconstruction with PTFE tubular graft died suddenly 1 month after surgery, and the cause of death was suspected to be acute pulmonary embolism as a result of graft thrombosis. The remaining 15 patients died of local recurrence or distant metastasis of RCC. Fifteen patients survive after surgery, with metastatic disease in five and without in 10. Overall 1-, 5-, and 10-year survival rates, including two cases of operation-related death, were 70%, 44%, and 26.4%, respectively (Fig 2). One- and 5-year survival rates were 81.3% and 52.9% for stage III and 50% and 31.2% for stage IV (Fig 3). A statistically significant correlation was found between surgical staging and survival (P =.049). Patients without lymph node metastasis had a significant survival advantage over those with lymph node metastasis (Fig 4, P =.022). There was no significant difference in survival based on the presence or absence of synchronous lung metastasis (Fig 5, P =.291). The degree of local extension of the tumor (T factor) or the level of tumor thrombus (V factor) did not tend to influence survival (Figs 6 and 7); however, statistical rank test could not be performed. DISCUSSION In 1913 Berg 12 first reported nephrectomy and venacavotomy for RCC extended into the IVC. Since this report, radical nephrectomy with vena caval thrombectomy has become a standard treatment for this entity. The operative mortality rates previously reported ranged from 2.7% to 13% 9,10,13-15 ; those were very compatible with our results. In this series we encountered two cases (5.9%) of operationrelated death; one of them was caused by massive bleeding, and the other one was suspected to be caused by intraoper-

792 Tsuji et al April 2001 Fig 2. Overall survival rate with Kaplan-Meier method. Fig 3. Cumulative survival based on surgical stage with Kaplan-Meier method (log-rank test =.049). Dashed lines indicate SE > 10%. ative pulmonary tumor embolism. The former one was the initial case of this series, and blunt thrombectomy with balloon catheter was performed without complete exposure of the retrohepatic IVC. We now consider that tumor thrombus must be resected under complete exposure and isolation of the IVC under liberal use of CPB. Blunt thrombectomy with balloon catheter is now never performed because of IVC injury, pulmonary embolism, and tumor residual on the IVC wall. The latter patient died of pulmonary tumor embolism, which is also one of the fatal complications of this surgery. 16,17 TEE is valuable for intraoperative monitoring of IVC tumor thrombus and can

Volume 33, Number 4 Tsuji et al 793 Fig 4. Comparison of survival based on lymph node status with Kaplan-Meier method (log-rank test =.022). Dashed lines indicate SE > 10%. Fig 5. Comparison of survival based on distant metastasis with Kaplan-Meier method (log-rank test =.291). Dashed lines indicate SE > 10%. diagnose pulmonary embolism with disappearance of the tumor head, dislodging of the tumor into pulmonary arteries, or any sign of right heart dysfunction. 18 For the prevention of pulmonary tumor embolism, gentle surgical maneuver and intraoperative hemodynamic stability may be necessary. When the tumor 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 suprarenal IVC are not yet established. Duckett et al 19 indicated that suprarenal IVC resection without venous replace-

794 Tsuji et al April 2001 Fig 6. Comparison of survival based on degree of tumor extension with Kaplan-Meier method. Dashed lines indicate SE > 10%. ment can be well tolerated because collateral pathways such as the lumbar and epigastric pathways, renal veins, and vertebral system are well developed by chronic occlusion of the IVC. On the other hand, some authors suggested that venous reconstruction after suprarenal IVC resection is advisable because large dissection of a retroperitoneal tumor and a thoracoabdominal incision can both interrupt ascending venous pathways and carry the risk of major venous insufficiency. 2,20 In this series, venous reconstruction was performed in all cases to prevent unexpected venous insufficiency. When the wall defect was less than one third of the circumference of the IVC, cavotomy was closed directly. When the wall defect was more than one third of the circumference of the IVC, venous reconstruction was performed with PTFE patch or tubular graft. Total replacement of the IVC with PTFE graft was first reported by Sarti 21 in 1970. Since this report, the IVC reconstruction with PTFE tubular graft for malignant tumors was reported with excellent long-term patency. 2-4,20,22 However, we are prudent to perform total circumferential replacement of the IVC with prosthetic graft, because one of our patients died of pulmonary embolism after graft thrombosis during the followup period. Patch angioplasty with PTFE or autogenous pericardium is now our first choice for the IVC repair if the venous wall is not entirely invaded. Techniques of caval control during thrombectomy will vary depending on the location of tumor thrombus. If the tumor thrombus is still limited below the level of hepatic veins (Va and Vb), vascular isolation can be obtained by clamps of the IVC and the contralateral renal vein without any circulatory support. If the tumor thrombus is present above the level of hepatic veins (Vc), some circulatory supports or hepatic vascular exclusion (HVE) is necessary during cross-clamping of the IVC. HVE is a well-established technique for vascular isolation during liver resection. With this technique, bleeding through hepatic veins during cavotomy is remarkably reduced and IVC tumor can be resected with excellent exposure. If hypotension induced by venous return decreases as a result of HVE, venovenous bypass is available to stabilize hemodynamic conditions. 22,23 Some investigators recommend the use of HVE during resection of IVC tumor, because it makes the control of the most inaccessible portion of IVC easier and safer. 2,15,24,25 For example, Nesbitt et al 15 indicated that even some of intraatrial tumor thrombus could be resected without CPB. Their maneuver was to gently palpate the tumor at the cavoatrial junction and manipulate the tumor into the suprahepatic IVC; a vascular cross-clamp was then applied across the IVC below the cavoatrial junction; cavotomy was made and tumor thrombus was removed under HVE. However, small veins that drain directly into retrohepatic IVC, such as short hepatic veins, inferior phrenic veins, vertebral veins, or right adrenal veins, sometimes become a major collateral system as a result of chronic IVC occlusion. Backflow from these veins brings unexpected bleeding from cavotomy even in the presence of HVE. To preserve the blood from lumbar and hepatic veins, some investigators recommend the use of a cell-saving device associated with HVE procedure. 13,15 The use of a cell-saving device may reduce total amount of blood transfusion; however, it is

Volume 33, Number 4 Tsuji et al 795 Fig 7. Cumulative survival based on extension level of tumor thrombus with Kaplan-Meier method. Dashed lines indicate SE > 10%. helpless against intraoperative massive bleeding with hypotension. Thus, we routinely use normothermal CPB without cardiac arrest during the resection of IVC tumor extending above the level of hepatic veins. With the use of CPB, the bleeding can be sucked and immediately returned in the CPB circuit. The use of CPB stabilizes hemodynamic conditions during IVC isolation and brings complete tumor resection and venous reconstruction. The risk of CPB use may be a possibility of tumor dissemination; however, some reports indicated that the use of extracorporeal circulation during the resection of tumor thrombus in the IVC did not affect long-term survival. 9,15 Some previous studies have indicated that there was worse survival in the group of patients with a more proximal extension of tumor thrombus of RCC. 9,14,26,27 Sosa et al 27 reported a 2-year survival rate of 80% in patients with retrohepatic IVC thrombus compared with only 21% in those with suprahepatic thrombus. Skinner et al 14 indicated a 5-year survival rate of 35% in patients with infrahepatic IVC thrombus compared with 18% and 0% in those with retrohepatic IVC or intra-atrial thrombi, respectively. On the other hand, some reports indicated that the level of the thrombus had no statistically significant impact on survival. 15,28-30 Glazer and Novick 31 reviewed 18 patients with RCC with IVC thrombus extending into the right atrium and concluded that their long-term survival was not significantly different from that reported for patients with RCC and infrahepatic or retrohepatic IVC thrombi. Hatcher et al 13 indicated that prognosis in such cases was determined by the pathologic stage of the RCC and by the presence or absence of vena caval wall invasion but not by the level of tumor thrombus extension. In our patients the level of tumor thrombus (V factor) did not tend to influence survival. A statistically significant correlation was found between surgical staging and survival; the presence of lymph node metastasis was an especially potent risk factor for late death. Surgical indication for RCC with distant metastasis is controversial. Montie et al 9 found that a patient with metastatic disease was 2.76 times more likely to die than a patient without metastasis. Suggs et al 32 reviewed 26 patients who underwent radical nephrectomy and vena caval thrombectomy, and all five patients who had distant metastatic disease did not survive beyond 12 months. Swierzewski et al 30 reported surgical prognosis in 100 cases of RCC extending into the IVC and concluded that the presence of metastatic disease or nodal involvement precludes consideration of vena caval surgery because its survival rate was significantly poor. On the other hand, Nesbitt et al 15 indicated that distant metastases did not significantly alter the prognosis although lymph node metastases had an associated poor survival rate. Naitoh et al 33 reviewed 31 patients with RCC with tumor extension into the IVC and concurrent distant metastasis. The overall 5-year survival rate was 17% after aggressive surgical resection and postoperative immunotherapy with interleukin-2; interestingly, patients in whom metastasis was limited to the lung had significantly better survival than those with metastasis to other sites. In our series, concurrent distant metastasis was recognized in seven cases (20.6%), and all of them were lung

796 Tsuji et al April 2001 metastases. Their overall 5-year survival rate was 42.9%, and presence of synchronous distant metastasis did not significantly alter survival. This excellent result is suspected to be contributed to by postoperative immunotherapy with interferon; however, effectiveness of adjuvant immunotherapy could not be proved in this series. We agree with the conclusion of Nesbitt et al 15 that all patients with RCC and IVC tumor thrombus should be considered for operation. Even in the presence of metastatic disease, prolonged survival is expected in patients who have partial or complete responses to immunotherapy after surgery. Furthermore, removal of the primary neoplasm along with the IVC tumor thrombus has some palliative roles: improvement of clinical symptoms, removal of an immediately life-threatening focus of disease, and reduction of tumor mass before immunotherapy. CONCLUSIONS Surgical prognosis in patients with RCC extending into the IVC was determined by the staging of the tumor, especially lymph node status, and not by the extension level of tumor thrombus or the presence of concurrent distant metastasis. The use of CPB is recommended for the resection of tumor thrombus extending over the diaphragm. REFERENCES 1. Tsuji Y, Yamashita C, Wakiyama H, Toyoda Y, Yoshida M, Sugimoto T, et al. Surgical treatment for transvenous tumor extension into the heart: four cases. J Vasc Surg 1998;27:740-4. 2. Huguet C, Ferri M, Gavelli A. Resection of the suprarenal inferior vena cava: the role of prosthetic replacement. Arch Surg 1995;130:793-7. 3. Kumada K, Shimahara Y, Fukui K, Itoh K, Morikawa K, Ozawa K. Extended right hepatic lobectomy: combined resection of inferior vena cava and its reconstruction by eptfe graft. Acta Chir Scand 1988;154: 481-3. 4. Risher WH, Arensman M, Ochsner JL, Hollier LH. 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