Disease Speci c Survival as Endpoint of Outcome for Bladder Cancer Patients Following Radical Cystectomy
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1 European Urology European Urology ) 440±448 Disease Speci c Survival as Endpoint of Outcome for Bladder Cancer Patients Following Radical Cystectomy JuÈrgen E. Gschwend a,b,*, Philipp Dahm c, WilliamR. Fair b a Department of Urology, University of Ulm, Prittwitzstrasse 43, Ulm, Germany b Urology Service, Memorial Sloan-Kettering Cancer Center, New York, NY, USA c Division of Urology, Duke University Medical Center, Durham, NC, USA Accepted 11 February 2002 Abstract Objective: To directly compare disease speci c and overall survival as endpoints in the outcome analysis of a large number of cystectomy patients and to de ne predictors for survival. Materials and Methods: We retrospectively analyzed the records of 686 patients who underwent bilateral pelvic lymph node dissection PLND) and radical cystectomy from 1980 to 1990 at Memorial Sloan-Kettering Cancer Center. Results: Disease speci c survival characterized a clearly more favorable patient outcome than overall survival in the entire patient population as well as patients with organ con ned OC) and non-organ-con ned disease NOC): 10- year disease speci c and overall survival rates for patients with OC disease P3a), negative nodes or NOC P3b) were 72.9% versus 49.1%, 61.7% versus 40.8% and 33.3% versus 22.8%, respectively. In node positive N ) patients 10-year disease speci c and overall survival rates were 27.7% and 20.9%, respectively. In a multivariate analysis organ con nement and nodal status were the strongest independent predictors of disease speci c survival in all patient categories. However, strati cation according to organ con nement and nodal status revealed additional prognostic parameters. Conclusion: Organ-con ned bladder cancer translates into high disease speci c survival rates following radical cystectomy. Outcome is best characterized by disease-speci c survival versus overall survival, which underestimates the impact of treatment in patients with favorable tumor and nodal stage. Subgroup analysis of patients with organ con nement and nodal status identi ed additional prognostic variables within the more favorable patient categories not apparent in the entire population. The poor prognosis of patients with NOC and/or N tumors emphasized the importance of future randomized trials in which such strati cation variables may be of value. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Bladder cancer; Radical cystectomy; Disease-speci c survival; Prognostic factors 1. Introduction Pelvic lymph node dissection PLND) and radical cystectomy is considered to be the gold standard in regard to local tumor control and ultimate cure of cancer and is regarded to be superior to radiationtherapy or organ conserving surgery [1], whereas chemotherapy offers the only viable but limited option in the treatment of distant metastasis. * Corresponding author. Tel.: ; Fax: address: juergen.gschwend@medizin.uni-ulm.de J.E. Gschwend). Most previous studies analyzing outcome of bladder cancer patients have used actuarial overall survival [2±6] rather than disease speci c survival [7] as the endpoint to assess patient outcome. This appears reasonable if the observed mortality in such patients can largely be attributed to their progressive bladder cancer rather than other underlying medical conditions. As previously suspected [8,9] however, differences in disease speci c and overall survival can be signi cant and are likely to be more important in patients with organ con ned OC) disease in whomthe bene t of radical cystectomy is expected to be greatest. We therefore sought to directly compare disease speci c /02/$ ± see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S )00060-X
2 J.E. Gschwend et al. / European Urology ) 440± and overall actuarial survival of a large patients series undergoing radical cystectomy to test whether disease speci c survival may serve as a better endpoint for clinical trials. Several investigators have con rmed the importance of tumor and nodal stage as prognostic variables both in a univariate and multivariate analysis [4,6,7]. Meanwhile controversy remains as to whether further predictors of outcome exist which may serve as important strati cation variables for adjuvant therapy. The identi cation of such prognostic factors may be obscured in higher disease stages with or without positive nodes and more apparent in patient's with less advanced disease stages and long-termfollow-up. In this study therefore we directly compare for the rst time the long-term disease speci c and overall actuarial survival of a large series of well characterized cystectomy candidates with or without additional treatment. In order to de ne speci c predictors of disease speci c survival a multivariate analysis of prognostic variables was performed for the entire patient population as well within patient categories grouped by organ con nement of the tumor and nodal status. 2. Material and methods We retrospectively analyzed a total of 762 patients with primary epithelial carcinoma of the bladder undergoing bilateral PLND and radical cystectomy at the Memorial Sloan-Kettering Cancer Center between 1980 and Of the 762 patients %) were included in the nal analysis as only incomplete basic information was available in 76 10%). Indication for cystectomy was biopsyproven, muscle invasive disease and/or rapid relapse after transurethral resection with or without concomitant carcinoma in situ Cis). Muscle invasion determined elsewhere was routinely con- rmed by repeat transurethral resection at Memorial Hospital. PLND and radical cystectomy in male patients and anterior exenteration in female patients was performed as described previously [8,9]. Pathologic tumor and lymph node stage were determined by an experienced uropathologist and classi ed according to the 1992 TNM system as described by the American Joint Committee on Cancer Staging AJC) [10] and the International Union Against Cancer UICC) [11]. The histological grade was established according to the Ash grading system. Further pathologic features included in the analysis were the tumor growth pattern papillary versus solid), tumor multifocality and vascular invasion in a subset of 390 patients. A substantial percentage of patients received additional treatment in the form of systemic neoadjuvant, adjuvant or palliative chemotherapy and/or preoperative irradiation. 115 patients received chemotherapy only, 236 patients had radiotherapy only mostly as part of a planned integrated approach <2500 rads) in a neoadjuvant manner and 146 patients underwent radio- and chemotherapy in addition to cystectomy. Previous analysis of the impact of neoadjuvant and adjuvant treatment in this patient population, which was mainly administered outside of controlled trials, failed to demonstrate any signi cant impact on outcome [9]. Patients were generally followed with physical examination at 2±6 month intervals and yearly CT or MRI scan, bone scan, chest X-ray, intravenous pyelography and urine cytology. Both disease speci c and overall survival was used as the end point of outcome in this study. Disease speci c survival was calculated as the number of years fromcystectomy to the date of death frombladder cancer or to the last follow up date for patients still alive. To eliminate a potential staging error in patients receiving neoadjuvant chemotherapy or repeated transurethral resections we used the most advanced stage either assessed frompreoperative staging transurethral resections or radical cystectomy specimen for survival analysis. Great efforts were placed on the accurate determination of the cause of death or patients status. Death of disease was recorded when patients had documented progressive disease during follow-up and their death was attributable to further disease progression. Death without evidence of disease was recorded when the last follow-up examination revealed no evidence of disease or when autopsies were available and no evidence of disease was demonstrated. A unknown cause of death was recorded if no recent follow-up information or autopsy reports were available. 47/ %) patients in whomthe cause of death 41) or disease status 6) could not be determined were censored for the purpose of the survival calculations Table 1). Prognostic variables evaluated included the P-category, N-category, tumor grade, age, gender, tumor growth pattern, tumor type and vascular invasion. For assessment of microscopic vascular invasion, standard H&E staining as well as CD31 immunohistochemistry was performed. Data regarding vascular invasion were only available in a subset of 390 patients. Disease speci c survival and overall survival distributions were estimated using the Kaplan± Meier algorithm[12] and compared by the log rank test. Patients who died of other causes than bladder cancer were censored at the time of their death for the disease speci c survival analysis. Subsequently, these variables were entered into a multivariate analysis in a forward, stepwise manner using the Cox proportional Table 1 Status of 686 cystectomy cases strati ed according to P- and N-categories Category Alive with disease No evidence of disease Death of disease Death with disease Unknown cause of death Alive, unknown tumor status Patients status unknown Totals P-stage OC NOC N-stage N N
3 442 J.E. Gschwend et al. / European Urology ) 440±448 hazard model. Statistical analysis was performed using a commercial software package. For all statistical tests P-values <0.05 were considered signi cant. 3. Results Among the 686 patients with a mean age of ± 86) years eligible for survival analysis 312 patients 45.5%) were found to have organ-con ned disease and 374 patients 54.5%) non-organ-con ned NOC) disease. 193 patients 28.1%) had node-positive disease Table 2). Pure transitional cell carcinoma TCC) was present histologically in 597 patients 87.0%), pure adenocarcinoma ACA) in %) and pure squamous cell carcinoma SCC) in 19 patients 2.8%). TCC with concurrent ACA was present in %), with concurrent SCC in %), spindle cell carcinoma %) and small cell carcinoma in 4 patients 0.6%). The median length of follow-up of the entire population was 6.22 years Table 2). The percentage of patients with organ-con ned, node negative N0), NOC and node positive N ) disease that died of bladder cancer during the follow-up was 20.8%, 30.4%, 54.3% and 61.1%, respectively. The death rate due to other causes was 21.2%, 19.3%, 13.9% and 12%, respectively. Age and gender distribution among the four groups was not signi cantly different. Comparison of disease speci c and overall survival curves for the entire population found the diseasespeci c survival to describe a more favorable outcome Fig. 1). While the median disease-speci c survival time was not reached at over 14 years of follow-up, the median overall survival was 4.6 years. A subgroup analysis of patients by organ-con nement and nodal status found a substantial difference between diseasespeci c and overall survival rates, which was most pronounced in patients with OC disease or negative nodes Table 3 and Fig. 2A and C). In organ-con ned patients or patients with negative nodes the 10-year disease speci c survival rate versus the overall survival rate were 72.9% versus 49.1% and 61.7% versus 40.8%, respectively. In NOC patients the corresponding 10-year survival rates were 33.3% and 22.8%, respectively. N patients had 10-year disease and overall survival rates of 27.7% and 20.9%, respectively. Disease-speci c survival was subsequently chosen as the endpoint of the outcome analysis. Long-term disease speci c survival was calculated stage by stage Table 2 Clinical characteristics of 686 cystectomy patients Patients Disease speci c deaths Overall deaths Median follow-up years) All %) %) 6.22 P-stage OC %) %) 6.49 NOC %) %) 5.82 N-stage N %) %) 6.18 N %) %) 6.63 Tumor grade GI, GII %) %) 6.22 GIII %) %) 6.29 Age %) %) 7.45 > %) %) 5.57 Gender Female %) %) 6.30 Male %) %) 5.93 Focality Unifocal %) %) 6.11 Multifocal %) %) 6.76 Tumor growth pattern Papillary %) %) 6.29 Solid %) %) 6.35 Vascular invasion Absent %) %) 5.58 Present %) %) 6.29
4 J.E. Gschwend et al. / European Urology ) 440± Fig. 1. Kaplan±Meier overall and disease speci c survival function in 686 cystectomy patients. The difference between both groups was statistically signi cant. for the organ-con ned and NOC category accounting for nodal status. Within the category of organ-con ned tumors P3a, negative nodes) increasing pathological tumor stage correlated with a decreased disease-speci c survival P ˆ 0:004) Fig. 3). The disease speci c survival of patients with deep muscle invasion P3a) was signi cantly P ˆ 0:001) more favorable Fig. 4) than that of patients with extension into the perivesical Table 3 Comparison of overall and disease speci c survival rates strati ed according to organ-con ned OC) disease, NOC disease, negative and positive lymph nodes Category Interval years) Disease speci c survival %) Overall survival %) All patients OC Tumors T3a) NOC Tumors >T3a) Negative lymph nodes N0) Positive lymph nodes N ) Declining statistical differences between overall and disease speci c survival with increasing tumor burden. fat P3b). NOC disease stage P3b or P4b with negative nodes, as well as N disease was associated with a poor disease speci c survival Fig. 5). However, patients with Cis of the prostatic urethra or ducts and otherwise OC disease meanwhile had a favorable outcome that was comparable to that of OC tumor stages. A separate analysis of disease speci c survival comparing clinical stage, pathological stage and most advanced stage did not demonstrate any substantial differences between the 10-year survival rates using pathological stage versus the worst stage disease speci c survival rates of 71:3 3:1% versus 72:9 3:1% for OC disease stages). However, the use of the clinical stage resulted in a substantially lower 10-year survival rate 55:6 2:5%) compared to P-stage or worst stage. A univariate analysis of prognostic variables of disease-speci c survival was performed for the entire population as well as separately within the categories of organ-con ned, NOC, N0 and node-positive disease. Tumor stage and nodal stage were the most important prognostic variables for the entire population as well as for patients strati ed by their nodal status and tumor stage, respectively Table 4). Vascular invasion, which was analyzed within a subset of 390 patients, was equally identi ed as a signi cant variable in all categories except patients with N disease. Additional
5 444 J.E. Gschwend et al. / European Urology ) 440±448 Fig. 2. Kaplan±Meier disease speci c and overall survival estimations according to A) OC, B) NOC, C) N0 and D) N ). adverse prognostic factors identi ed for the entire population n ˆ 686) were a tumor grade of 3 P ˆ 0:015), an age >65 years P ˆ 0:034) and a pattern of solid tumor growth P < 0:001). In the subgroups, additional prognostic variables were as well identi ed in the prognostic categories of OC disease and negative node status with favorable outcome, however not in NOC and N patients. These factors were tumor grade, age and gender. Patients with a tumor grade of three experienced a shorter disease-speci c survival than patients with a well or moderately differentiated tumor grade 1 and 2). Fig. 3. Disease speci c survival strati ed according to P-category in patients with organ-con ned disease P3a). Differences between groups were statistically signi cant P ˆ 0:004). Fig. 4. Kaplan±Meier curves of disease speci c survival comparing patients with P3a and P3b disease. Differences between groups were statistically signi cant P ˆ 0:001).
6 Fig. 5. Disease speci c survival strati ed according to P-category in patients with NOC disease P3b). Differences between groups were statistically signi cant P ˆ 0:001). Table 4 Univariate analysis of predictors of disease speci c survival based on the entire study population, patients with OC, NOC disease, N0 and N patients Category All patients OC NOC N0 N P-stage N-stage ± Tumor grade NS) NS) Age NS) NS) Gender 0.40 NS) NS) NS) Focality 0.07 NS) 0.72 NS) 0.51 NS) 0.07 NS) 0.94 NS) Tumor type NS) NS) Vascular invasion a NS) Events Censored Total a Based on a subset of 390 patients. Table 5 Multivariate analysis of predictors of disease speci c survival based on the entire study population, patients with OC, NOC, N0 and N ) patients Category All patients OC NOC N0 N P-stage NS) N-stage ± Tumor grade 0.47 NS) 0.09 NS) 0.55 NS) 0.31 NS) 0.60 NS) Age NS) Gender 0.47 NS) 0.11 NS) 0.93 NS) NS) Focality 0.89 NS) 0.24 NS) 0.6 NS) 0.85 NS) 0.98 NS) Tumor type NS) 0.05 NS) NS) Vascular invasion a b c d 0.2 NS) Events Censored Dropped Total a Replaces tumor type P ˆ 0:317) as independent predictor. b Replaces N-stage P ˆ 0:137) and P-stage P ˆ 0:105) as independent predictors. c Replaces age P ˆ 0:280) as independent predictor. d Replaces age P ˆ 0:147), gender P ˆ 0:954), and tumor type P ˆ 0:065) as independent predictors.
7 446 J.E. Gschwend et al. / European Urology ) 440±448 A female gender and an age <65 years were found to be favorable prognostic criteria. However, tumor growth pattern was not signi cant in patients with OC tumors. In a multivariate regression analysis tumor stage, nodal stage, age and tumor type were the only independent prognostic variables in the presence of other signi cant covariables that were signi cant in the total patient population Table 5). Vascular invasion analyzed in those 390 patients in whomthis information was available was an independent predictor of disease speci c survival in all categories P < 0:001) except patients with node-positive disease P ˆ 0:2). Age was an independent factor in OC, NOC and N0 but not N patients. Gender P ˆ 0:03) and tumor type P ˆ 0:018) were additional independent variables in N0 patients. Tumor stage was the only additional independent covariable besides N-stage in N patients P ˆ 0:011). 4. Discussion A majority of studies analyzing the outcome of bladder cancer patients have used overall survival rather than disease-speci c survival as the endpoint of analysis [2±6]. In patient populations with advanced pathological tumor and nodal stage the majority of deaths may be attributed due to distant metastasis and overall survival may serve as an appropriate surrogate endpoint of disease-speci c survival. Studies using disease speci c survival as the endpoint may require higher numbers of patients to reveal statistically signi cant differences between groups, because patients dying of unrelated causes are censored at their date of death. However, as we have shown in this study, overall survival approximates disease-speci c survival only if the proportion of cancer unrelated deaths is small. As surgery improves survival, increasing differences between disease-speci c and overall survival can be demonstrated proportionally with improved outcome. In our study this was re ected by profound differences when comparing the disease-speci c and overall survival of patients with NOC and OC disease as well as N and N0 disease. The 10-year disease speci c and overall survival rates in organ-con ned disease were 72.9% and 49.1%, respectively. In N0 patients the 10-year disease speci c and overall survival rates were 61.7% and 40.8%, respectively. These differences of 23.8% and 20.9%, respectively in the 10- year survival rates highlights the importance of using disease-speci c survival as the endpoint of outcome analysis. While most authors have found the pathological tumor and nodal stage to be strong predictors of long-termsurvival, there is no consensus whether additional independent prognostic variables may signi cantly impact on the outcome of cystectomy patients. Only few published studies with extended follow-up have a large enough number of events, i.e. disease speci c deaths to allow a meaningful statistical analysis in this regard. In an analysis of prognostic variables in 130 patients Soloway et al. [4] found the N-stage to be the only independent predictor of overall survival. In a thorough analysis of both clinical and pathologic prognostic factors in 369 patients, Bassi et al. [6] identi ed only P-stage and N-stage as independent predictors of overall survival in a multivariate analysis. Frazier et al. [7] on the other hand, based on the outcome analysis on a larger series of 531 patients, found age, grade, and the presence of positive margins to be additional independent predictors of disease speci c survival. In this study we performed a detailed analysis of outcome variables of a large numbers of patients in both, the entire population as well as in subgroups of patients grouped by pathologic stage and nodal stage. In a comprehensive analysis not previously reported in this formwe found that different independent variables impacted upon the outcome within each patient category Table 5). The observed differences were most profound when comparing the prognostic variables of patients with organ-con ned disease P-stage, N-stage, age and vascular invasion), N0 disease P-stage, age, gender, tumor type and vascular invasion) and N disease only P-stage as covariable). Our results suggest that the number of patients, the length of follow-up and the P- and N-stage distribution of the population analyzed, signi cantly in uences the role of secondary prognostic variables. Notably, the series reported by Frazier et al. [7], which identi es four additional prognostic variables, is comparatively large and includes a high proportion of patients with a favorable prognostic P-stage 88% Ta-T3a) and N-stage 89% N0) compared to the study by Bassi et al. [6] 67% Tis-T3a, 79% N0). These differences underscore the need to clearly de ne the population at risk in respect to P- and N-stage when discussing prognostic variables. The identi cation of such important prognostic variables may prove critical for the patient strati cation in future randomized clinical trials. While a detailed analysis of the outcome of only a subset of N bladder cancer patients has previously been published we here present a detailed outcome analysis of all patients [8,9]. A decrease in disease speci c survival was demonstrated stage by stage.
8 J.E. Gschwend et al. / European Urology ) 440± Overall, about 70% of patients with organ-con ned disease were free of tumor at 10 years, whereas tumor extension into perivesical fat or extravesical disease predicted a poor prognosis. There was a statistically signi cant difference in the outcome of patients with pt3a deep muscle invasion) and pt3b perivesical fat invasion). This nding validates the new TNM nomenclature of 1997 with its distinction between pt2b deep muscle invasion) and pt3a miscroscopic invasion of perivesical fat). Meanwhile, patients with Cis of the urethra or prostatic ducts pt4a cis ) and otherwise OC disease have a more favorable outcome than other pt4-stages including patients with prostatic stromal invasion pt4a stroma ). These ndings are in accordance with those of others; it has been clari ed, that stromal invasion of the prostate arising intraurethrally decreases survival signi cantly compared to Cis in the urethra or prostatic ducts with otherwise OC disease [13]. This further suggests, that super cial involvement of the prostate should be regarded as an OC tumor stage with favorable prognosis. Some potential limitations to the design and interpretation of this study deserve mention. First, this represents a retrospective analysis of a patient population treated over a 10-year period of time and subject to different regimens of additional treatment. While our previous analysis of the impact of concurrent adjunct chemo- or radiation-therapy failed to demonstrate a signi cant impact on overall or disease speci c survival some occult bias from confounding therapies cannot be excluded and must be considered [9,14]. Second, stage migration, selection bias including that created by performing subgroup analysis and inaccurate staging may have in uenced these results. Finally, while the de nition of disease speci c survival was crucial and great efforts were placed on the accurate assignment of the cause of death, a small number of inaccuracies cannot be ruled out completely. However, given the high levels of statistical signi cance encountered in this analysis we feel the conclusions made are well supported. As radical cystectomy and PLND remains the gold standard in the treatment of muscle-invasive bladder cancer with excellent outcomes in patients with OC, N0 tumors, the long-term outcome of patients with locally advanced disease remains poor [2,3,5,6]. In regards to adjunct chemotherapy, the addition of neoadjuvant treatment has so far not demonstrated superiority over cystectomy alone [15]. Adjuvant chemotherapy has shown ef cacy in patients with locally advanced disease in few prospective studies [16±19]. However, the de nitive impact of adjuvant chemotherapy on survival was left unanswered by these trials due to several limitations in the study design and methodology used. Future randomized studies of such treatment strategies should not only use T- and N-stage as strati cation variables but also include additional prognostic criteria such as vascular invasion for appropriate patient subsets. 5. Conclusion In patients undergoing radical cystectomy diseasespeci c survival appears to be a more accurate predictor of outcome than overall survival, in particular when favorable disease stages are present. In this analysis, pathological tumor and nodal stage were con rmed to represent strong independent prognostic variables of disease speci c survival emphasizing the value of the 1997 TNM systemto stratify patients for adjuvant treatment modalities. In subsets of patients with favorable outcome further prognostic variables were identi ed not signi cant in the overall population. This nding underscores the need for large, wellcharacterized patient populations with extended follow-up when discussing the value of prognostic variables and the impact of any applied therapy. The poor prognosis of patients with NOC and/or node-positive disease emphasizes the importance of future randomized trials to test the true ef cacy of established and new adjunct therapies in combination with radical cystectomy. Acknowledgements We thank Dr. Josef HoÈgel, Assistant Professor, Department of Biometry and Medical Documentation, Faculty of Medicine, University of Ulmfor helpful discussions and assistance with the statistical analysis. Supported by Deutsche Forschungsgemeinschaft Gs 8/5-1 and 8/5-2 DFG), Bonn, Germany. References [1] Montie JE. Against bladder sparing surgery. J Urol 1999;162:452±7. [2] Pagano F, Bassi P, Galetti TP, Meneghini A, Milani C, Artibani W, et al. Results of contemporary radical cystectomy for invasive bladder cancer: A clinicopathological study with an emphasis on the inadequacy of the tumor, nodes and metastases classi cation. J Urol 1991;145:45±50.
9 448 J.E. Gschwend et al. / European Urology ) 440±448 [3] Lerner SP, Skinner DG, Lieskovsky G, Boyd SD, Groshen SL, Ziogas A, et al. The rationale for en bloc pelvic lymph node dissection for bladder cancer patients with nodal metastases: Long termresults. J Urol 1993;149:758±65. [4] Soloway MS, Lopez AE, Patel J, Ying L. Results of radical cystectomy for transitional cell carcinoma of the bladder and the effect of chemotherapy. Cancer 1993;73 7):1926±31. [5] Freeman JA, Esrig D, Stein JP, Simoneau AR, Skinner EC, Chen SC, et al. Skinner DG. Radical cystectomy for high risk patients with super cial bladder cancer in the era of orthotopic urinary reconstruction. Cancer 1995;76 5):833±9. [6] Bassi P, Ferrante GD, Piazza N, Spinadin R, Carando R, Pappagallo G, et al. Prognostic factors of outcome after radical cystectomy for bladder cancer: A retrospective study of a homogeneous patient cohort. J Urol 1999;161:1494±7. [7] Frazier HA, Robertson JE, Dodge RK, Paulson DF, et al. The value of pathologic factors in predicting cancer-speci c survival among patients treated with radical cystectomy for transitional cell carcinoma of the bladder and prostate. Cancer 1993;71:3993± [8] Vieweg J, Gschwend JE, Herr HW, Fair WR. The impact of primary stage on survival in patients with lymph node positive bladder cancer. J Urol 1999;161:72±6. [9] Vieweg J, Gschwend JE, Herr HW, Fair WR. Pelvic lymph node dissection can be curative in patients with node positive bladder cancer. J Urol 1999;161:449±54. [10] American joint committee on cancer. In: Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ, editors. Manual for staging of cancer. 4th ed. Philadelphia PA): JB Lippincott, pp. 199±200. [11] TNM classi cation of malignant tumors. In: Hermanek P, Sobin LH, editors. International Union Against Cancer, 4th ed. New York: Springer, p [12] Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J AmStat Assoc 1958;53:457±81. [13] Esrig D, Freeman JA, Elmajian DA, Stein JP, Chen S, Groshen S, et al. Transitional cell carcinoma involving the prostate with a proposed staging classi cation for stromal invasion. J Urol 1996;156:1071±6. [14] Vieweg J, Whitmore Jr WF, Herr HW, Sogani PC, Russo P, Sheinfeld J, et al. The role of pelvic lymphadenectomy and radical cystectomy for lymph node positive bladder cancer. Cancer 1994;73 12):3020±8. [15] BA06/30894 trial. Neoadjuvant cisplatin, methotrexate and vinblastine chemotherapy for muscle-invasive bladder cancer: A randomized controlled trial. Lancet 1999;354:533±40. [16] Skinner DG, Daniels JR, Russell CA, Lieskovsky G, Boyd SD, Nichols P, et al. The role of adjuvant chemotherapy following cystectomy for invasive bladder cancer: A prospective comparative trial. J Urol 1991;145:459±64. [17] StoÈckle M, Meyenburg W, Wellek S, Voges GE, Rossmann M, Gertenbach U, et al. Adjuvant polychemotherapy of non-organcon ned bladder cancer after radical cystectomy revisited: long-term results of a controlled prospective study and further clinical experience. J Urol 1995;153:47±52. [18] Freiha F, Reese J, Torti FM. A randomized trial of radical cystectomy versus radical cystectomy plus cisplatin, vinblastine and methotrexate chemotherapy for muscle-invasive bladder cancer. J Urol 1996;155:495±500. [19] Sylvester R, Sternberg C. The role of adjuvant combination chemotherapy after cystectomy in locally advanced bladder cancer: What we do not know and why. Ann Oncol 2000;11 7):851±6.
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