Prognostic Value of Renal Vein and Inferior Vena Cava Involvement in Renal Cell Carcinoma

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1 european urology 55 (2009) available at journal homepage: Kidney Cancer Prognostic Value of Renal Vein and Inferior Vena Cava Involvement in Renal Cell Carcinoma Bernd Wagner a, *, Jean-Jacques Patard b, Arnaud Méjean b, Karim Bensalah b, Grégory Verhoest b, Richard Zigeuner c, Vincenzo Ficarra d, Jacques Tostain e, Peter Mulders f, Denis Chautard g, Jean-Luc Descotes b, Alexandre de la Taille h, Laurent Salomon h, Tommaso Prayer-Galetti i, Luca Cindolo j, Antoine Valéri b, Nicolas Meyer a, Didier Jacqmin a, Hervé Lang a,b a Department of Urology, Strasbourg University Hospital, Nouvel Hôpital Civil, Strasbourg, France b CCAFU, Rennes, Paris Necker, Grenoble, Brest, Strasbourg, France c Department of Urology, Graz University Hospital, Graz, Austria d Department of Urology, Verona University Hospital, Verona, Italy e Department of Urology, Saint-Etienne University Hospital, Hôpital Nord, Saint-Etienne, France f Department of Urology, Nijmegen University Hospital, Nijmegen, The Netherlands g Department of Urology, Angers University Hospital, Angers, France h Department of Urology, Hôpital Henri Mondor, Créteil, France i Department of Urology, Padua University Hospital, Padua, Italy j Department of Urology, Benevento University Hospital, Benevento, Italy Article info Article history: Accepted July 23, 2008 Published online ahead of print on August 5, 2008 Keywords: Kidney cancer Renal cell carcinoma Prognosis Venous thrombus Renal vein involvement Inferior vena cava involvement Abstract Background: The prognostic significance of venous tumor thrombus extension in patients with renal cell carcinoma (RCC) is a matter of many controversies in the current literature. Objective: To evaluate the prognostic role of inferior vena cava (IVC) involvement in a large series of pt3b and pt3c RCCs. Design, setting, and participants: A total of 1192 patients from 13 European institutions underwent a radical nephrectomy for pt3b and pt3c RCC between 1982 and The patients were evaluated in a retrospective manner. Age, gender, clinical symptoms, Eastern Cooperative Oncology Group (ECOG) performance status, TNM stage, tumor size, adrenal invasion, perinephric fat invasion, histological type, and Fuhrman grade were reviewed. The log-rank and Cox uni- and multivariate regression analyses were used to evaluate prognostic factors for overall survival. Measurements: Overall survival and prognostic factors for overall survival in patients with RCC extending to the renal vein (RV) or to the IVC. Results and limitations: The median follow-up was 61.4 mo ( mo). The mean age was 63.2 yr. The mean tumor size was 8.9 cm. Group 1 (Gr 1) included 933 patients with a renal vein tumor thrombus (78.3%), Group 2 (Gr 2) included 196 patients with a subdiaphragmatic IVC tumor thrombus (16.4%), and Group 3 (Gr 3) included 63 patients * Corresponding author. Department of Urology, Place de l Hôpital, Strasbourg, 67091, France. address: bernd.wagner@chru-strasbourg.fr (B. Wagner) /$ see back matter # 2008 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi: /j.eururo

2 european urology 55 (2009) with a supradiaphragmatic IVC tumor thrombus (5.3%). Median survival was 52 mo for Gr 1, 25.8 mo for Gr 2, and 18 mo for Gr 3. In univariate analysis, Gr 1 had a significantly better overall survival than Gr 2 ( p < 0.001) and Gr 3 ( p 0.001). No significant difference in survival was noted between Gr 2 and Gr 3 ( p = 0.613). Prognostic factors for overall survival in univariate analysis were clinical symptoms ( p < 0.001), tumor size ( p < 0.001), perinephric fat invasion ( p < 0.001), Fuhrman grade ( p < 0.001), histological type ( p = 0.021), lymph node invasion ( p < 0.001), and distant metastasis ( p < 0.001). Independent prognostic factors in multivariate analysis were tumor size ( p = 0.013), perinephric fat invasion ( p = 0.003), lymph node invasion ( p < 0.001), distant metastasis ( p < 0.001), and IVC invasion ( p = 0.008). Conclusions: The level of tumor thrombus in the IVC does not significantly affect longterm overall survival in patients with renal cell carcinoma. The overall survival was statistically different for patients with a tumor thrombus in the RV compared to those with IVC involvement. This has to be considered for the next revision of the TNM system, and the pt3b and pt3c stages have to be redesigned. # 2008 European Association of Urology. Published by Elsevier B.V. All rights reserved. 1. Introduction Renal cell carcinoma (RCC) represents 2 3% of all solid cancer, and it is the third most common cancer of the urinary tract, with an incidence of 6 12 cases per people in Western countries [1]. It is more frequent in men than in women (1.5:1), with a peak incidence between 60 and 70 yr of age [2]. One of the characteristics of RCC is its propensity to invade the venous system, with extension into the renal vein (RV) and the inferior vena cava (IVC) in 23% and 7%, respectively [1]. To predict survival in patients with RCC, prognostic factors were established. They can be classified as anatomical, histological, clinical, and molecular factors. Anatomic factors include tumor size, renal capsule invasion, adrenal involvement, venous invasion, and lymph node and distant metastasis [2], which were gathered by the TNM stage classification system of the UICC (Union International Contre le Cancer) as pathological stage. Pathological stage is the strongest predictor of survival in patients with RCC [3 5]. The TNM classification is regularly revised [6]. The current 2002 TNM stage classification system, summarized in Table 1, is generally recommended for clinical and scientific use, but it is unclear whether it is optimal for the prediction of survival in patients with RCC, and refinements remain to be performed, especially for locally advanced RCC [2]. The current TNM classification combines RCC with RV and IVC invasion below the diaphragm together as stage pt3b, whereas tumors with IVC involvement above the diaphragm are classified as stage pt3c. The prognostic significance of the level of venous extension in RCC is the subject of many controversies in the current literature [5,7 14] The aim of the present study was to evaluate the prognostic value of venous involvement according to the extent of IVC invasion and to test the independent prognostic value of IVC invasion in a large series of pt3b and pt3c tumors. Table 1 The 2002 TNM staging classification system T- Primary tumor Tx Primary tumor cannot be assessed T0 No evidence of primary tumor T1 Tumor 7 cm in greatest dimension, limited to the kidney T1a Tumor 4 cm in greatest dimension, limited to the kidney T1b Tumor >4 cm but 7 cm in greatest dimension T2 Tumor >7 cm in greatest dimension, limited to the kidney T3 Tumor extends into major veins or directly invades adrenal gland or perinephric fat tissues but not beyond Gerota s fascia T3a Tumor directly invades adrenal gland or perinephric fat tissues but not beyond Gerota s fascia T3b Tumor directly invades renal vein(s) or its segmental branches or the vena cava below the diaphragm T3c Tumor grossly extends into vena cava or its wall above diaphragm T4 Tumor directly invades beyond Gerota s fascia N- Regional lymph nodes NX Regional lymph nodes cannot be assessed N0 No regional lymph node metastasis N1 Metastasis in a single regional lymph node N2 Metastasis in more than one regional lymph node M- Distant metastasis MX Distant metastasis cannot be assessed M0 No distant metastasis M1 Distant metastasis

3 454 european urology 55 (2009) Table 2 Patient characteristics Group 1 (n = 933) Group 2 (n = 196) Group 3 (n = 63) Age <60 yr 256 (27.4%) 58 (29.6%) 14 (22.2%) >60 yr 677 (72.6%) 138 (70.4%) 49 (77.8%) Gender Female 315 (33.8%) 73 (37.2%) 21 (33.3%) Male 618 (66.2%) 123 (62.8%) 42 (66.7%) Symptoms (28.5%) 26 (13.9%) 6 (10.2%) (71.5%) 161 (86.1%) 53 (89.8%) Missing data Histopathologic category Clear cell 815 (93.6%) 167 (91.3%) 57 (98.3%) Papillary 24 (2.8%) 9 (4.9%) 1 (1.7%) Chromophobe 13 (1.5%) 3 (1.6%) 0 (0.0%) Collecting duct 13 (1.5%) 1 (0.6%) 0 (0.0%) Other 6 (0.7%) 3 (1.6%) 0 (0.0%) Missing data Fuhrman grade I 28 (3.3%) 8 (4.4%) 0 (0.0%) II 268 (31.2%) 23 (12.8%) 14 (25.5%) III 431 (50.2%) 99 (55.0%) 31 (56.4%) IV 132 (13.4%) 50 (27.8%) 10 (18.2%) Missing data Tumor size 4 cm 37 (4.0%) 1 (0.5%) 0 (0.0%) >4 7 cm 259 (28.3%) 31 (16.2%) 14 (23.0%) >7 cm 619 (67.7%) 159 (83.3%) 47 (77.1%) Missing data T3a Perinephric fat invasion (50.8%) 66 (43.4%) 20 (46.5%) (49.2%) 86 (56.6%) 23 (53.5%) Missing data Adrenal gland invasion (93.5%) 139 (85.3%) 44 (91.7%) 1 40 (6.5%) 24 (14.7%) 4 (8.3%) Missing data N (Regional lymph nodes) N0 713 (81.3%) 136 (72.3%) 43 (69.4%) N+ 164 (18.7%) 52 (27.7%) 19 (30.7%) Nx M (Distant metastasis) M0 680 (73.2%) 135 (69.6%) 45 (71.4%) M+ 249 (26.8%) 59 (30.3%) 18 (28.6%) Mx ECOG PS (58.2%) 59 (46.5%) 18 (50.0%) (41.8%) 68 (53.5%) 18 (50.0%) Missing data ECOG PS, Eastern Cooperative Oncology Group performance score. 2. Methods 2.1. Patient selection In order to better assess the respective prognostic value of RV and IVC involvement, 1192 patients with RV (n = 933) or IVC (n = 259) involvement by a RCC tumor thrombus who had been treated by radical nephrectomy at 13 European academic centers were included in this retrospective study Study parameters Gender, age (younger or older than 60 yr), and symptoms at initial presentation (absent or present) were recorded. Tumor

4 european urology 55 (2009) size was evaluated on fixed pathological specimens. Histological subtype, determined according to the 1997 World Health Organization (WHO) Heidelberg classification, was split into clear cell renal cell carcinomas (ccrcc) versus non-ccrccs. Tumor nuclear grade was determined according to the Fuhrman system. TNM stage was determined according to the 2002 version. Stage pt3b was defined as a tumor thrombus extension into the renal vein or its segmental musclecontained branches or the vena cava below the diaphragm. Stage pt3c was defined as a tumor thrombus extension into the vena cava above the diaphragm. No differentiation between venous wall invasion and venous thrombus extension was performed. Perinephric fat and adrenal invasions were specifically recorded. Performance status was assessed according to the Eastern Cooperative Oncology Group performance score (ECOG PS) scale. No data were collected concerning surgical technique Statistical methods We identified three prognostic groups: Group 1 (Gr 1) included tumors with invasion limited to the RV, Group 2 (Gr 2) included tumors with RV and IVC invasion below the diaphragm, and Group 3 (Gr 3) included tumors with IVC extension above the diaphragm. Survival was determined from the date of nephrectomy to the date of last follow-up or death. For univariate analysis, survival differences were evaluated by Kaplan-Meier estimates and log rank test. Multiple predictors of outcome were evaluated by Cox proportional hazard analysis. Differences were considered statistically significant when p < Results 3.1. Patients, tumors, and follow-up There were 783 males (65.7%) and 409 females (34.3%). Mean age was 63.2 yr (19 96), mean tumor size was 8.93 cm (1 26). Patient characteristics are summarized in Table 2. Median follow-up was 61.4 mo ( ). Only four patients were lost to follow-up. Among 1188 patients with pt3b-c tumors, 650 were dead at last follow-up (54.7%), including 545 patients who died of RCC in a median time of 13.8 mo following nephrectomy. Among 545 patients who died from RCC, 48 patients (4.3%) died in the perioperative period (first month after surgery), including 23 (3%) in the RV group and 25 (9.65%) in the IVC group ( p = 0.289). No difference in perioperative mortality was found between IVC invasion below (18 out of 196 = 9.2%) and above the diaphragm (7 out of 96 = 7.3%; p = 0.88). In 12 cases, the cause of death was unknown, whereas 93 patients died from non cancer-related causes. The median follow-up time in 538 patients who were still alive at last follow-up was 61.4 mo ( ) Survival predictive factors Median survival time was 52.0, 25.8, and 18 mo for Gr 1, Gr 2, and Gr 3, respectively. In univariate analysis, Gr 1 patients had a significantly better survival outcome than Gr 2 ( p < 0.001) and Gr 3 patients ( p 0.001; Fig. 1). There was no significant survival difference between Gr 2 and Gr 3 ( p = 0.613). Additionally, univariate analysis showed that clinical symptoms ( p < 0.001), histological subtype ( p = 0.021), Fuhrman grade ( p < 0.001), tumor size ( p < 0.001), fat invasion ( p < 0.001), adrenal invasion ( p < 0.001), nodal invasion ( p < 0.001), and distant metastasis ( p < 0.001) were statistically significant predictors factors for overall survival. Age, gender, and ECOG performance status did not significantly affect overall survival. Fig. 1 Global survival of renal cell carcinoma (RCC) with venous involvement: Group 1 versus Group 2 versus Group 3.

5 456 european urology 55 (2009) Table 3 Prognostic factors in multivariate analysis Prognostic factor In multivariate analysis (summarized in Table 3), the presence of IVC invasion ( p = 0.008) remained an independent predictive factor. Other variables which were retained as independent prognostic parameters were: tumor size ( p = 0.013), fat invasion ( p =0.003), lymph node invasion ( p < 0.001), and distant metastasis ( p < 0.001). Age, gender, clinical symptoms, histological type, Fuhrman grade, and performance status failed to show a statistically significant impact on overall survival in multivariate analysis. In order to determine if the three groups could be combined into a two-group model (with Gr 2 and Gr 3 merged as a single level), we compared the threegroup model (Gr 1, Gr 2, Gr 3) versus the two-group model (Gr 1, Gr 2 + Gr 3). The performance of the two models was similar. This suggests that both coding systems were acceptable. Therefore, we chose to use the two-level coding scheme. When excluding patients with nodal or distant metastasis (N+, M+), only tumor size ( p = 0.05) remained a predictive factor independently of IVC invasion. Perinephric fat invasion was an independent predictive factor only in Gr 1 patients. Symptoms and ECOG performance status had to be excluded because of an insufficient number of patients. 4. Discussion Multivariate analysis IVC invasion p = Tumor size p = Fat invasion p = Lymph node metastasis p < Distant metastasis p < IVC, inferior vena cava. The 2002 primary TNM classification for T3b RCC does not differentiate between patients with tumor involvement of the RV and the IVC below the diaphragm. The prognostic impact of the level of tumor thrombus has been extensively analysed, but the discussion of the prognostic value of IVC invasion is controversial [2,7 18]. Some reports have demonstrated decreased survival in patients with tumor thrombus involving the IVC [5,7,13,14,17,18]. Other studies have not identified level of venous invasion as a negative prognostic indicator. They support the current TNM classification [2,8,10 12,15,16]. The present study is, to our knowledge, the largest of RCC including tumors with venous involvement. Our data indicate that patients with T3b RCC and only RV involvement had a significantly better overall survival compared with T3b RCC extending into the IVC, and this was true in metastatic (N+, M+) and nonmetastatic (N0, M0) disease. No significant difference was found according to the level of IVC involvement. Moinzadeh and Libertino found similar results, and they proposed redefinition of pt3b RCC [14]. Their results are similar to those of the Mayo Clinic published by Blute at al, who found no difference in survival by thrombus level among patients with IVC involvement [13]. Hatcher demonstrated the pejorative value of tumor thrombus invasion of the wall of the IVC [10]. This feature is relatively rare and barely studied. Our studies did not differentiate between tumor thrombus with or without invasion of the IVC wall because we lack this information in many pathological reports. As in other studies, lymph node and distant metastases were an independent prognostic factor, and their presence is known to reduce survival significantly not only in patients with venous involvement [1,5,7,11 14,16 18,20]. In several studies, lymph node involvement had a greater impact on the outcome than the extent of tumor thrombus [11,13,16]. On the contrary, Monti et al concluded that survival did not depend on lymph node status if the IVC was invaded [21]. Multivariate analysis of several series showed that distant metastasis decreased the outcome rather than the extent of tumor thrombus [13,17]. In our study, there was no difference in incidence of distant metastasis at the initial presentation between patients with RV only compared with those with IVC involvement. Glazer et al found no difference in the incidence of lymph node or distant metastasis at initial presentation between patients with an atrial thrombus compared with those with a lower level of IVC involvement [11]. Consistent with other series [22,23], we showed that tumor size is an independent prognostic factor on overall survival in metastatic (N+, M+) and nonmetastatic (N0, M0) disease. Our findings support the role of tumor size as a very important predictor of outcome. The importance of tumor invasion in the perinephric fat and its negative impact on prognosis for patients with RCC invading the RV and IVC had been recently described by Leibovich in 2005 and more recently by Ficarra [3,4,7]. By reclassifying locally advanced RCC in three subgroups with significantly different prognoses, Ficarra et al proposed a new staging system of pt3a, pt3b, and pt4 tumors [3]:

6 european urology 55 (2009) Group one (pt3a ) included patients with perirenal fat invasion or renal vein thrombosis or thrombosis within the inferior vena cava below the diaphragm, group two (pt3b ) included patients with tumors with renal vein thrombosis or thrombosis within the vena cava below the diaphragm and concomitant perirenal fat invasion, and, finally, group three (pt4 ) included patients with adrenal gland or Gerota fat invasion or thrombosis within the vena cava above the diaphragm [3]. Similar to other studies, our series showed that perinephric fat invasion was an independent prognostic factor in RCC with RV involvement, but not in nonmetastatic RCC (N0, M0) with IVC involvement [11,17]. Unlike the results of Ficarra, we did not find any significant difference in prognosis based on the level of IVC thrombosis. Although some RCC with vein invasion can be cured surgically, recurrence developed in a significant proportion of patients, as recently shown in the review paper by Kirakali and van Poppel [9]. This is why it is also essential to select patients with high risk of recurrence and progressive disease. According to Kirkali and van Poppel s review, this population may benefit in the near future from adjuvant treatments with target agents [9]. Several investigators have combined various prognostic factors with the aim of finding predictors of outcome. One of them, the UCLA Integrated Staging System (UISS), incorporates TNM stage, tumor grade, and ECOG performance status, parameters which were also available in our study [25]. In our series, Fuhrman grade and ECOG performance status were only prognostic predictors in univariate analysis, whereas the UCLA staging system classified pt3 tumors depending on Fuhrman grade and ECOG performance status in different subgroups. Stage pt3 tumors with ECOG0 and any Fuhrman grade or pt3 tumors with ECOG+ and Fuhrman grade I were classified in UISS group 2, whereas pt3 tumors with ECOG+ and Fuhrman grade II IV were classified in UISS group 3 [24]. We support the hypothesis that RCC with vein invasion is associated with higher Fuhrman grade, as shown in Table 1 [12,25,26]. Contrary to other publications, Fuhrman grade did not influence global survival as an independent prognostic factor in our study [5]. Contrary to other series, ECOG performance status failed to be an independent prognostic factor in multivariate analysis, but 35 53% missing data limited the value of our results [26,27]. Perioperative mortality was, in most cases, caused by bleeding, thromboembolic complications, and septicaemias [15,16]. In our studies, the perioperative mortality was 3% and 9.6% for RV and IVC thrombus, respectively. Perioperative mortality of tumors with IVC thrombus varied in other series between 3% and 10% [10,13,15,16,19,28,29]. In a study by Staehler and Brkovic, it goes up to 40% if IVC thrombus extended to the IVC above the diaphragm [15]. More recently, Cianco et al published a series of 66 patients with tumor thrombus in the IVC. They performed an exclusive transabdominal approach with liver mobilisation, permitting a low perioperative mortality of 4.5% (3 patients of 66) [29]. In our multicenter study (13 centers), we did not assess the different surgical techniques, but it may be very heterogeneous due to the long period of inclusion (20 yr) and the different experience of each institution in RCC surgery. In our study, we found no significant difference between IVC invasion below and above the diaphragm, which were 9.2% and 7.3% ( p = 0.88), respectively. Blute et al reported a decrease in perioperative mortality in tumors with IVC invasion (3.8%) treated from 1990 to 2000 compared to patients treated from 1970 to 1989, where the perioperative mortality was 8.1% [13]. Perioperative mortality depends also on comorbidities [13,15]. Bissada et al reported a higher perioperative mortality in patients with metastasis (33%) versus patients without metastasis (2%) [16]. Nevertheless, Zisman et al described similar postoperative morbidity in these two groups [30]. In conclusion, perioperative mortality can be influenced by surgical techniques. Our results are consistent with those described in the literature. 5. Conclusions Tumor size, perinephric fat invasion, and lymph node and distant metastasis are important and independent prognostic factors in RCC with vein involvement. IVC invasion of any level decreases, significantly and independently, the prognosis of patients with RCC. The distinction between pt3b and pt3c RCC needs to be reevaluated in a venous invasion above and below the junction of the RV with the IVC in the next version of the TNM system. Author contributions: Bernd Wagner had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Lang. Acquisition of data: Wagner, Patard, Méjean, Bensalah, Verhoest, Zigeuner, Ficarra, Tostain, Mulders, Chautard, Descotes, de la Taille, Salomon, Prayer-Galetti, Cindolo, Valéri. Analysis and interpretation of data: Wagner, Lang. Drafting of the manuscript: Wagner. Critical revision of the manuscript for important intellectual content: Jacqmin, Lang, Patard.

7 458 european urology 55 (2009) Statistical analysis: Meyer. Obtaining funding: None. Administrative, technical, or material support: None. Supervision: Lang, Patard, Méjean. Other (specify): None. Financial disclosures: I certify that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None. Funding/Support and role of the sponsor: None. References [1] Campbell S, Novick A, Bukowski R. Treatment of locally advanced renal cell carcinoma. In: Campbell S, Walsh P, editors. Urology. Philadelphia, PA: W. B. Saunders Co.; p [2] Ljungberg R, Stenling R, Osterdahl B, Farrelly E, Åberg T, Roos G. Vein invasion in renal cell carcinoma: impact on metastatic behaviour and survival. J Urol 1995;154: [3] Ficarra V, Novara G, Iafrate M, et al. Proposal for reclassification of the TNM staging system in patients with advanced (pt3 4) renal cell carcinoma according to the cancer-related outcome. Eur Urol 2007;51: [4] Ficarra V, Galfano A, Guille F, et al. A new staging system for locally advanced (pt3-4) renal cell carcinoma: a multicenter European study including 2000 patients. J Urol 2007;178: [5] Haferkamp A, Bastian PJ, Jacobi H, et al. Renal cell carcinoma with tumor thrombus extension into the vena cava: prospective long-term follow-up. J Urol 2007;177: [6] Gospodarowicz MK, Miller D, Groome PA, Greene FL, Logan PA, Sobin LH. The process for continuous improvement of the TNM classification. Cancer 2004;100:1 5. [7] Leibovich BC, Cheville JC, Lohse CH, et al. Cancer specific survival for patients with pt3b renal cell carcinoma can the 2002 primary tumor classification be improved? J Urol 2005;173: [8] Klatte T, Pantuck A, Riggs S, et al. Prognostic factors for renal cell carcinoma with tumor thrombus extension. J Urol 2007;178: [9] Kirkali Z, van Poppel H. A critical analysis of surgery for kidney cancer with vena cava invasion. Eur Urol 2007;52: [10] Hatcher PA, Anderson EE, Paulson DF, Carson CC, Robertson JE. Surgical management and prognosis of renal cell carcinoma invading the vena cava. J Urol 1991;145:20 3. [11] Glazer A, Novick A. Long-term followup after surgical treatment for renal cell carcinoma extending into the right atrium. J Urol 1996;155: [12] Kim LH, Zisman A, Han KR, Figlin RA, Bellegrun AS. Prognostic significance of venous thrombus in renal cell carcinoma. Are renal vein and inferior vena cava involvement different? J Urol 2004;171: [13] Blute M, Leibovitch B, Lohse C, Cheville J, Zincke H. The Mayo Clinic experience with surgical management, complications and outcome for patients with renal cell carcinoma and venous thrombus. BJU 2004;94: [14] Moinzadeh A, Libertino JA. Prognostic significance of tumor thrombus level in patients with renal cell carcinoma and venous tumor thrombus extension. Is all T3b the same? J Urol 2004;171: [15] Staehler G, Brkovic D. The role of radical surgery for renal cell carcinoma with extension into the vena cava. J Urol 2000;163: [16] Bissada N, Yakout H, Babanouri A, et al. Longterm experience with management of renal cell carcinoma involving the inferior vena cava. Urology 2003;61: [17] Gettman MT, Boelter CW, Cheville JC, Zincke H, Bryant SC, Blute ML. Charlson co-morbidity index as a predictor of outcome after surgery for renal cell carcinoma with renal vein, vena cava or right atrium extension. J Urol 2003;169: [18] Klaver S, Joniau S, Suy R, Oyen R, van Poppel H. Analysis of renal cell carcinoma with subdiaphragmatic macroscopic vein invasion (T3b). BJU Int 2008;101: [19] Parekh DJ, Cookson MS, Chapman W, et al. Renal cell carcinoma with renal vein and inferior vena caval involvement: clinicopathological features, surgical techniques and outcome. J Urol 2005;173: [20] Libertino JA, Zinman L, Watkins Jr E. Long-term results of resection of renal cell carcinoma with extension into inferior vena cava. J Urol 1987;137:21 4. [21] Montie JE, el Ammar R, Pontes JE, et al. Renal cell carcinoma with inferior vena cava tumor thrombi. Surg Gynecol Obst 1991;173:107. [22] Rabbani F, Hakimian P, Reuter VE, Simmons R, Russo P. Renal vein or inferior vena caval extension in patients with renal cortical tumors: impact of tumor histology. J Urol 2004;171: [23] Bretheau D, Koutani A, Lechevallier E, Coulange C. A French national epidemiology survey on renal cell carcinoma. Oncology Committee of the Association Française d Urologie. Cancer 1998;82:538. [24] Pantuck AJ, Zisman A, Belldegrun A. Biology of renal cell carcinoma: changing concepts in classification and staging. Semin Urol Oncol 2001;19:72 9. [25] Ficarra V, Righetti R, Martignoni G, et al. Prognostic value of renal cell carcinoma nuclear grading: multivariate analysis of 333 cases. Urol Int 2001;67: [26] 0nu M, Fujimoto Y, Takada T, et al. Prognostic factors for survival of patients after curative surgery for renal cell carcinoma: multivariate analysis of 483 cases. Int J Clin Oncol 2004;9: [27] Motzer RJ, Mazumbar M, Bacik J. Survival and prognostic stratification of 670 patients with advanced renal cell carcinoma. J Clin Oncol 1999;17: [28] Zini L, Haulon S, Leroy X, et al. Endoluminal occlusion of the inferior vena cava in renal cell carcinoma with retroor suprahepatic caval thrombus. BJU Int 2006;97:

8 european urology 55 (2009) [29] Ciancio G, Livingstone AS, Soloway M. Surgical management of renal cell carcinoma with tumor thrombus in the renal and inferior vena cava: the University of Miami experience in using liver transplantation techniques. Eur Urol 2007;51: [30] Zisman A, Pantuck AJ, Chao DH, et al. Renal cell carcinoma with tumor thrombus: is cytoreductive nephrectomy for advanced disease associated with an increased complication rate? J Urol 2002;168: Editorial Comment on: Prognosis Value of Renal Vein and Inferior Vena Cava Involvement in Renal Cell Carcinoma Paul Russo Memorial Sloan Kettering Cancer Center, 1275 York Avenue, New York, New York 10021, United States RussoP@MSKCC.org The authors present data from 13 centers and 1192 patients accumulated over a 21-yr period to define the prognosis of renal tumors invading the renal vein and inferior vena cava (IVC) [1]. Most patients had a renal vein thrombus (78.3%), 16.4% had subdiaphragmatic IVC thrombus, and 5.3% had a supradiaphragmatic IVC thrombus. Despite the large number of patients in this study, 47% of the patients already had evidence of poor prognostic systemic disease in the form of metastatic nodes (n = 235, 19.7%) and distant metastases (n = 326, 27.3%), and even a highly successful operation on the renal tumor and its thrombus would not affect the poor outcome for those patients. When the authors analyzed their data in the N0 M0 patients, only tumor size predicted vascular invasion and overall survival. For patients with N+ and M+ disease, resection of the kidney tumor and its thrombus should be considered either a cytoreductive nephrectomy and/or a tumor metastasectomy [2] with patient survival ultimately dependent upon the presence of associated risk factors [3] and response to systemic agents. This large surgical series is notable for a perioperative mortality of 3% for tumors involving the renal vein and 9.6% for tumors involving the IVC, which is most consistent with the contemporary literature and again reminds us that these are a very challenging group of surgical patients. Elements of the individual tumor (size, tumor grade, perinephric fat extension, regional and distant metastases) have the greatest bearing on survival. There is a reason for optimism for future patients with locally advanced, massive renal tumors with or without renal vein and IVC extension. Our new understanding of the molecular biology of renal cell carcinoma has led to the development and the US Food and Drug Administration approval of new systemic chemotherapy agents, including the multitargeted tyrosine kinase (TKI) inhibitors (sunitinib, sorafenib) and mammalian target of rapamycin (mtor) kinase inhibitors (temsirolimus, RAD001). These agents have been effective in inducing partial remissions and prolonging survival in metastatic renal cancer and previously treated metastatic renal cancer patients [4,5] and are more effective than cytokines when compared in randomized trials. For these difficult, poor prognostic surgical patients, numerous neoadjuvant and adjuvant clinical trials utilizing these agents have been launched in the United States and Europe in hopes of improving prognosis. References [1] Wagner B, Patard J-J, Méjean A, et al. Prognostic value of renal vein and inferior vena cava involvement in renal cell carcinoma. Eur Urol 2009;55: [2] Russo P, Snyder M, Vickers A, Kondagunta V, Motzer R. Cytoreductive nephrectomy and nephrectomy/complete metastasectomy for metastatic renal cancer. TSW Urology 2007;2: [3] Eggener SE, Yossepowitch O, Pettus JA, Snyder ME, Motzer RJ, Russo P. Renal cell carcinoma recurrence after nephrectomy for localized disease. Predicting survival from time of recurrence. J Clin Oncol 2006;24: [4] Bukowski RM, Wood LS. Renal cell carcinoma: state of the art diagnosis and treatment. Clin Oncol 2008;11:9 21. [5] O Brien F, Motzer R, Russo P. Sunitinib therapy in renal cell carcinoma. BJU Int 2008;101: DOI: /j.eururo DOI of original article: /j.eururo

9 460 european urology 55 (2009) Editorial Comment on: Prognostic Value of Renal Vein and Inferior Vena Cava Involvement in Renal Cell Carcinoma Ziya Kirkali Dokuz Eylul University, School of Medicine, Izmir 35340, Turkey While most patients with localized renal cell carcinoma (RCC) can be cured with surgery alone, the prognosis of patients with locally advanced disease is worse because a subset of those patients develops either local or systemic recurrences. The outcome of patients with renal vein and inferior vena cava (IVC) involvement and the relationship of extent and level to prognosis are still debatable [1]. In this paper by Wagner et al, 1192 patients are assessed for the prognostic role of the level of thrombus in IVC [2]. The authors should be congratulated for their efforts to define the role of the extent of IVC involvement in outcome for a large group of patients [2]. The data involved a retrospective series of patients from 13 European institutions treated within a rather long period of 20 yr with a median follow-up of 5 yr; thus, the reader should bear in mind that it is not a prospective study. Because it is a multicenter series, the surgical techniques and adjuvant and salvage therapies varied substantially according to the experience of each surgeon and center, as did the time when patients were treated. The majority of the patients had tumor in the renal vein (78.3%); the authors found that the median survival for those patients was 52 mo [2].If the thrombus extends to the IVC but below the diaphragm, survival was halved. The median survival for those with a thrombus above the diaphragm was only 18 mo. On multivariate analysis, it appears that tumor size, perinephric fat invasion, and lymph node and distant metastases are independent prognostic factors. The importance of perinephric fat invasion has also been shown in other studies [3]. The level of thrombus in the IVC did not have any impact on survival [2]. To my surprise, Fuhrman grade was not an independent prognosticator on multivariate analysis, but this may be due to the lack of central pathology review. Had Wagner et al performed a pathology review, they could have also evaluated the impact of microscopic vascular invasion on outcome, which is also important [4]. I think the impact of this paper is twofold. First, the authors rightly state that the current TNM classification does not differentiate the renal vein invasion from the IVC involvement. They propose to revise the TNM classification, and I concur with their proposal: T3b as tumor thrombus in the renal vein and T3c as IVC involvement irrelevant of the level. Second, I think the information derived from this series might aid in identifying those patients who are likely to progress (ie, if the thrombus extends into the IVC or if there are other bad prognostic factors). Those patients are the ideal candidates for randomizing in clinical trials for adjuvant therapies with current medical treatments in RCC. Indeed, we have to increase our efforts to help those patients with locally advanced RCC. References [1] Kirkali Z, van Poppel H. A critical analysis of surgery for kidney cancer with vena cava invasion. Eur Urol 2007;52: [2] Wagner B, Patard J-J, Méjean A, et al. Prognostic value of renal vein and inferior vena cava involvement in renal cell carcinoma. Eur Urol 2009;55: [3] Ficarra V, Novara G, Iafrate M, et al. Proposal for reclassification of the TNM staging system in patients with advanced (pt3 4) renal cell carcinoma according to the cancer-related outcome. Eur Urol 2007;51: [4] Sevinc M, Kirkali Z, Yorukoglu K, et al. Prognostic significance of microvascular invasion in localized renal cell carcinoma. Eur Urol 2000;38: DOI: /j.eururo DOI of original article: /j.eururo

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