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Ann Thorac Surg 1997;63:1592-1599
© 1997 The Society of Thoracic Surgeons
Departments of Thoracic and Cardiovascular Surgery and Urology, The University of Texas M. D. Anderson Cancer Center, Houston, Texas
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Abstract |
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 TopFootnotes Abstract IntroductionMaterial and MethodsSurgical TechniqueStagingStatistical MethodsResultsCommentReferences |
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Methods. From January 1989 to January 1996, 37 patients with renal cell carcinoma and inferior vena cava tumor thrombus underwent surgical resection. The 27 men and 10 women had a median age of 57 years (range, 29 to 78 years). Thirty-six patients presented with symptoms; 21 had hematuria. Distant metastases were present in 12 patients. Tumor thrombi extended to the infrahepatic inferior vena cava (n = 16), the intrahepatic inferior vena cava (n = 16), the suprahepatic inferior vena cava (n = 3), and into the right atrium (n = 2). All tumors were resected by inferior vena cava isolation and, when necessary, extended hepatic mobilization and Pringle maneuver, with primary or patch closure of the vena cavotomy. Cardiopulmonary bypass was necessary in only 2 patients with intraatrial thrombus.
Results. Complications occurred in 11 patients, and 1 patient died 2 days postoperatively of a myocardial infarction (mortality, 2.7%). Twenty patients are alive; overall 2- and 5-year survival rates were 61.7% and 33.6%, respectively. For patients without lymph node or distant metastases (stage IIIa), 2- and 5-year survival rates were 74% and 45%, respectively. The presence of distant metastatic disease (stage IV) at the time of operation did not have a significant adverse effect on survival, as reflected by 2- and 5-year survival rates of 62.5% and 31.3%, respectively. Lymph node metastases (stage IIIc) adversely affected survival as there were no long-term survivors.
Conclusions. Resection of an intracaval tumor thrombus arising from renal cell carcinoma can be performed safely and can result in prolonged survival even in the presence of metastatic disease. In our experience, extracorporeal circulatory support was required only when the tumor thrombus extended into the heart.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsSurgical TechniqueStagingStatistical MethodsResultsCommentReferences |
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Renal cell carcinoma (RCC) extends into the renal vein and inferior vena cava (IVC) as a thrombus of tumor in approximately 6% of all patients with this disease. Although such intravascular growth implies a heightened biologic behavior of the tumor, the presence of tumor thrombus associated with RCC has not been shown to be a determinant of survival [1–4]. For this reason, an aggressive approach to resection has been advocated for several decades and has remained the mainstay for treatment.
Management of such patients is primarily resection, with perioperative biotherapy in selected patients. Several different operations have been advocated depending on the proximal extent of tumor thrombus. When the thrombus is localized within the infrahepatic IVC, tumor 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.
Cardiopulmonary bypass improves control of immediate blood loss and with circulatory arrest allows for tumor removal in a bloodless field. But it is associated with higher overall blood loss, a greater rate of coagulopathy, and longer operative times [3–7]. Cardiopulmonary bypass is not usually required unless the tumor extends into the heart and requires atriotomy for removal. We reviewed our recent experience with patients having RCC with IVC tumor thrombi and herein report the results.
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsSurgical TechniqueStagingStatistical MethodsResultsCommentReferences |
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The levels of tumor thrombus were defined by four categories based on the extent of dissection required to remove the thrombus and are similar to those described by Neves and Zincke [8] (Fig 1
). In 9 patients, tumor thrombus extended from the renal vein into the infrahepatic IVC for 1 to 2 cm and required only local control of the IVC for extraction (level I). Seven patients had tumor thrombi that extended no further than the subhepatic IVC (level II). Sixteen patients had thrombus that extended into the intrahepatic IVC (level III). Three patients had thrombus that extended to the suprahepatic IVC but not into the atrium (also categorized as level III). The remaining 2 patients had intraatrial thrombi (level IV) and were the only patients requiring CPB for thrombectomy. Distant metastases were identified preoperatively in 12 patients.
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Surgical Technique |
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TopFootnotesAbstractIntroductionMaterial and MethodsSurgical TechniqueStagingStatistical MethodsResultsCommentReferences |
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). For patients with tumors having tumor thrombi limited to the infrahepatic IVC, an en bloc resection was performed if possible. If there was more extensive thrombus within the IVC but the thrombus was still limited to the infrahepatic IVC (level II), or if the thrombus extended higher, nephrectomy was performed first with ligation and amputation of the renal vein; the kidney was removed to allow better access and exposure of the IVC and the tumor thrombus was removed through an anterior cavotomy. For intra- or suprahepatic IVC tumor thrombi (level III) and intraatrial tumor thrombi (level IV), the liver required mobilization to provide access to the intrahepatic portion of the IVC. The liver was often completely and circumferentially mobilized so that only the major hepatic veins remained as the points of fixation of the liver to the IVC.
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For level III tumors, after complete hepatic mobilization, a Pringle maneuver was performed. After approximately 2 minutes to allow the liver to decompress, the infrarenal IVC, the contralateral renal vein, and the suprahepatic IVC were occluded, in that order. The patient was placed in the Trendelenburg position. The liver was rolled to the patient's left, and the IVC was opened along its anterolateral aspect to the level of the hepatic veins (Fig 3). The tumor thrombus was removed en bloc as completely as possible and adherent tissue was peeled from the endothelial surface directly or with the assistance of an endarterectomy spatula or Penfield dissector. In virtually all patients, the thrombus was not invading the caval wall but was adherent. If invasion of the wall occurred, it usually was localized to the renal vein orifice, a cuff of which was easily excised. Suture closure was begun proximally. When the IVC below the hepatic veins was closed, a vascular cross-clamp was applied immediately below the veins across the IVC and across the suture line, the Pringle maneuver was released, and the suprahepatic cross-clamp was removed; this minimized hepatic ischemia. Suturing of the IVC was continued, or if necessary, further thrombectomy and tumor debridement were performed. When the IVC was closed to the level of the infrarenal IVC, cross-clamps were repositioned to allow opening of the contralateral renal vein.
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Hepatic vein blood loss was reduced by use of a Pringle maneuver. No patient had the portal triad occluded for more than 30 minutes. A Greenfield filter or caval clip was placed in the infrarenal position if thrombus (benign clot or tumor thrombus) was present below this region before thrombectomy. In patients with complete caval occlusion, the vena cava was ligated below the renal vein.
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Staging |
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TopFootnotesAbstractIntroductionMaterial and MethodsSurgical TechniqueStagingStatistical MethodsResultsCommentReferences |
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Statistical Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsSurgical TechniqueStagingStatistical MethodsResultsCommentReferences |
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsSurgical TechniqueStagingStatistical MethodsResultsCommentReferences |
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Local caval resection was performed in 18 patients with patch closure being required in 4 patients. In most circumstances, caval resection was performed as part of the removal of a cuff of IVC around the renal vein. An IVC filter or clip was placed in 6 patients.
Median packed red blood cell transfusion requirement was 4.4 units for patients with level II thrombi, 4.9 units for those with level III thrombi, 9.6 units for those with level III thrombi in the suprahepatic region, and 10 units for those with level IV thrombi.
Among all 37 patients, 17 have died. Eight are alive with disease, and 12 are alive without disease. Mean follow-up time was 24 months (range, 3 days to 87.4 months). Overall 2- and 5-year survival rates were 61.7% and 33.6%. When the 1 perioperative death was excluded, the respective survival rates were 63.4% and 34.6%. The remainder of the survival analyses were performed to predict survival with the perioperative death excluded.
Including those with metastatic disease, 29 patients had complete resection of their primary tumors, and 7 had gross residual disease. Two-year survival rates were 69.5% and 38.1%, respectively (p = 0.188). When patients with metastatic disease were excluded from this analysis there was a significant difference in survival between patients with complete versus incomplete resection (p = 0.02) (Fig 4).
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). Only 1 of the 4 patients with stage IIIc disease is alive at 11.18 months. There was no statistical difference in survival between patients at various stages (p = 0.112), but the number of patients at stage IIIc was low. The 2- and 5-year survival rates for all patients with metastatic disease (lymph node metastases and distant metastases) were 49.1% and 24.6%; median survival in this group was 19.3 months.
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). The median follow-up time for patients with lymph node metastases was 6.84 months. The median follow-up time for patients without lymph node metastases was 54.31 months, although it should be noted that 62.1% of the patients remain censored. Eighteen patients remain alive in this group, with 2- year and 5-year survival rates of 73.4% and 40%, respectively.
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). When this group was compared with the 24 patients without distant metastatic disease (2- and 5-year survival rates of 64% and 39%, respectively), there was no significant difference between them (p = 0.88). Of the 12 patients with metastatic disease, 9 had no regional lymph node metastases. When survival times of these 9 patients were compared with those of all patients with lymph node metastases, there was a significant difference (p = 0.016) (Fig 7).
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). For the 2 patients with atrial tumors, the median survival was 6.84 months; 1 of these died 6.8 months postoperatively of metastatic disease, and the other is alive and disease free at 8.4 months.
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsSurgical TechniqueStagingStatistical MethodsResultsCommentReferences |
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In 1913, Berg [15] first described nephrectomy and vena cavotomy for RCC that extended into the IVC. Since this report, radical nephrectomy with vena cavotomy has become a safe and effective treatment of RCC with IVC thrombus, with operative mortality rates ranging from 2.7% to 13% (Table 1). Palliation can be immediately achieved by relief of the obstructing neoplasm, with expected 5-year survival from 30% to 72% (Table 1).
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). Contrast studies have been used in other series, but we have not found vena cavography to be additive to computed tomography and magnetic resonance imaging, and it heightens the risk of contrast-associated renal injury in a patient with one functioning kidney. Nine of our patients underwent renal arteriography for the purpose of renal artery embolization (a technique reported by Swanson and colleagues in 1980 [16]) 24 to 72 hours before operation in an attempt to reduce tumor vascularity and to contract the tumor thrombus.
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Preoperative anticoagulation was not used in our series as has been advocated by others to prevent sudden disseminated intravascular coagulopathy [4]. Depending on the degree of IVC occlusion, the presence and extent of hepatic vein obstruction, and the coexistence of an atrial thrombus with tricuspid valve blockage, the presence of a subtle coagulopathy or thrombocytopenia can be multifactorial. We have not encountered disseminated intravascular coagulopathy and have not been compelled to administer anticoagulants preoperatively. Subcutaneous heparin for deep venous thrombosis prophylaxis was administered perioperatively, and aspirin was prescribed after discharge. Warfarin was given postoperatively for 3 months in 1 patient.
We recommend nephrectomy and IVC thrombectomy as a technique that can be performed safely and completely without the need for CPB, except in cases where a level IV tumor thrombus exists. Other researchers advocate CPB with or without deep hypothermic circulatory arrest for both level III and level IV tumor thrombi for enhanced exposure and the ability to remove the tumor and its intracaval component in a bloodless field [6, 7, 17]. The disadvantages of deep hypothermic circulatory arrest include extended bypass times for blood rewarming, associated coagulopathy, and postoperative bleeding. Complications from bleeding or coagulopathy have been noted by several investigators (Table 2). Anticoagulation in a patient who has undergone an extensive retroperitoneal procedure and who has accessory venous collaterals from IVC obstruction increases the risk of intraoperative and postoperative bleeding. Deep hypothermic circulatory arrest further heightens the risk. The surgeon must consider the potential for bleeding and coagulopathy with CPB or CPB with deep hypothermic circulatory arrest, particularly when performed in conjunction with radical nephrectomy and lymph node dissection.
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In our series, shed blood from lumbar and hepatic veins was conserved by using a cell-saving device until the thrombus was fragmented. Although the cell-saving device in such cases may disseminate tumor, no evidence exists that shed cells from the tumor thrombus have an impact on survival [5, 6].
Lymph node involvement with metastatic disease and completeness of resection were found to be significant factors determining survival. The level of tumor thrombus, stage of disease, and the presence of distant metastases did not significantly influence survival.
In our patients with lymph node metastases, survival was worse than in those without nodal disease. Although Skinner [4] and Montie [6] and their associates noted no impact on survival in patients with or without lymph node metastases, other series corroborate our findings [2, 18–20]. Tongaonkar and colleagues [18] treated 47 patients with RCC with tumor thrombus extension into the renal vein or IVC. The 5-year survival was 50%, with a median survival of 4.35 years. Perinephric spread and lymph node metastases were significant prognostic factors affecting survival. Reissigl and colleagues [19] described their experience with 35 patients over a 20-year period of patients presenting with RCC extending into the IVC. Of the 23 patients who underwent resection, 15 patients had stage IIIa tumors and a 5-year survival rate of 62.5%. The remaining 8 patients had lymph node metastases and a mean survival rate of 15.5 months. In another series, Libertino and associates [20] found an overall 5-year survival of 59% with an overall 10-year survival of 47%. No patient with metastatic disease or nodal involvement survived beyond 5 years. Patients with no evidence of metastatic disease had a 60% survival rate with follow-up to 16 years. Hatcher and colleagues [2] found a 5-year survival of 62% for their patients with completely resected stage IIIa disease. For patients with lymph node metastases, the 5-year survival rate dropped to 17% (p = 0.004).
Patients with incomplete resections (excluding patients with metastatic disease) had a significantly worse prognosis. Similar findings have been shown by others and stress the importance of surgical eradication of disease [2, 4, 8]. Hatcher and colleagues [2], in a series of 44 patients with IVC wall invasion, noted that the prognosis was determined by the ability to perform a complete resection of the tumor, not by the level of tumor thrombus. They also showed the prognostic importance of complete resection in patients with nonmetastatic disease, as the 5-year survival rate drops from 57% to 0% (p = 0.02). Skinner and co-workers [4] identified the importance of complete resection by reporting a 34% 5-year survival in those patients undergoing a complete resection and a 1-year survival of only 8% in those who had incomplete resections. Furthermore, Neves and Zincke [8] noted a difference in 5-year survival between patients with complete thrombus removal (68%) and those with incomplete thrombus removal (17.5%).
The prognostic implication of the level of tumor thrombus is unclear, particularly when the thrombus extends into the atrium. Most series have not shown a significant difference in survival when the tumor thrombus remains below the atrium and therefore, have concluded that extension to the vena cava alone has a limited impact on survival [2, 4, 21, 22]. Cherrie [23], Novick [7], and Hatcher [2] and their colleagues have also reviewed their experiences in similar groups of patients with RCC and IVC thrombi and have not found the level of the tumor thrombus to impact survival. In the series by Montie and associates [6] patients with intrahepatic extension were 0.49 time less likely to die than those with renal or infrahepatic extension as determined by the Cox proportional hazards regression model. In the series reported by Marshall and co-workers [24] there was worse survival in the group of patients with a higher level tumor thrombus, but the difference was not statistically different. There may, however, be an influence on survival when the tumor thrombus extends into the atrium. Several investigators have noted a worse prognosis for patients with a tumor thrombus that extends into the atrium than for those with disease that remains within the IVC [4, 6, 24, 25]. In our group of patients, there was no significant difference in survival based on the level of tumor thrombus, although there was a trend toward improved survival in those patients who had a level I tumor thrombus.
Table 1 shows 3- and 5-year survival rates for patients with stage IIIa disease ranging from 30% to 72%. For those patients with metastatic disease to lymph nodes or distant sites, this table shows that survival was comparatively and consistently worse. Metastatic disease to lymph nodes or to distant sites seems to have an associated poor prognosis; most researchers note worse survival for such patients. Using the Cox proportional hazards regression model, Montie and colleagues [6] found that a patient with metastatic disease was 2.76 times more likely to die than a patient without metastases. However, in our series, although lymph node metastases had an associated poor survival rate, distant metastatic disease for unclear reasons did not significantly alter the prognosis. Several of our patients with distant metastases died within a short period after operation, but others have lived for more than 5 years with metastatic disease; 1 patient is alive at 87 months postoperatively. For those patients with metastatic disease and associated lymph node metastases (N1/2 and M1) compared with those without lymph node metastases (N0 M1), the survival rate was worse, which highlights the poor prognostic significance added by regional nodal disease. In few series is survival analyzed by comparing N1/2 M1 and N0 M1 disease; most patients with M1 disease are grouped together regardless of N status. But in the series by Neves and Zincke [8], N1 or N2 disease associated with M1 disease portended a poor prognosis.
Patients with metastatic RCC have a poor prognosis, an associated median survival of less than 1 year, and an associated 5-year mortality rate ranging from 80% to 100% [26, 27]. However, as seen in our group, there are some patients who, for unexplained reasons, have prolonged survival with metastatic disease [4, 8]. Some patients have disease that is uncharacteristically indolent, underscoring the unpredictability of its behavior. Other patients have disease that responds to biotherapy with interleukin or interferon that can affect a durable response, particularly in those with pulmonary metastases [2830]. In our group of patients with metastatic disease, several had partial or complete responses to perioperative biotherapy. Whether this influenced their outcome is unknown because the group was too small to analyze. Other than the reasons mentioned, we cannot provide a plausible explanation to account for the improved survival observed in these isolated cases.
Irrespective of the implications of distant disease and in consideration of the potential for a survival benefit, we believe that metastatic disease should not preclude operative intervention. We recommend removal of the primary neoplasm along with extraction of the IVC tumor thrombus to palliate symptoms, to remove an immediately life-threatening focus of disease, to reduce tumor burden before biologic therapy, and to reduce associated problems such as coagulopathies and hepatic dysfunction. With an acceptable overall operative mortality, with no reasonable alternative to management except expectant therapy, and with promising results from combinations of biologic therapy, operative intervention can be justified in selected patients.
In conclusion, all patients with RCC and IVC tumor thrombi should be considered for operation. Removal of the primary tumor and thrombus can be performed safely and can result in prolonged survival even in the presence of metastatic disease. In our experience, extracorporeal circulation is unnecessary except in those patients with intraatrial tumor thrombus.
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Footnotes |
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TopFootnotesAbstractIntroductionMaterial and MethodsSurgical TechniqueStagingStatistical MethodsResultsCommentReferences |
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Address reprint requests to Dr Nesbitt, Department of Thoracic and Cardiovascular Surgery, Box 109, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030.
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