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Re-examination of the Natural History of High-grade T1 Bladder Cancer using a Large Contemporary Cohort

Abstract

Introduction

High-grade T1 (HGT1) bladder cancer represents a clinical challenge in that the urologist must balance the risk of disease progression against the morbidity and potential mortality of early radical cystectomy and urinary diversion. Using two non-muscle invasive bladder cancer (NMIBC) databases, we re-examined the rate of progression of HG T1 bladder cancer in our bladder cancer populations.

Materials and Methods

We queried the NMIBC databases that have been established independently at the Atlanta Veterans Affairs Medical Center (AVAMC) and the University of Pennsylvania to identify patients initially diagnosed with HGT1 bladder cancer. Demographic, clinical, and pathologic variables were examined as well as rates of recurrence and progression.

Results

A total of 222 patients were identified; 198 (89.1%) and 199 (89.6%) of whom were male and non-African American, respectively. Mean patient age was 66.5 years. 191 (86.0%) of the patients presented with isolated HG T1 disease while 31 (14.0%) patients presented with HGT1 disease and CIS. Induction BCG was utilized in 175 (78.8%) patients. Recurrence occurred in 112 (50.5%) patients with progression occurring in only 19 (8.6%) patients. At a mean follow-up of 51 months, overall survival was 76.6%. Fifty two patients died, of whom only 13 (25%) patient deaths were bladder cancer related.

Conclusions

In our large cohort of patients, we found that the risk of progression at approximately four years was only 8.6%. While limited by its retrospective nature, this study could potentially serve as a starting point in re-examining the treatment algorithm for patients with HG T1 bladder cancer.

Urinary Bladder Neoplasms; Disease; Cystectomy; BCG Vaccine


INTRODUCTION

High-grade T1 bladder cancer (HGT1) represents a clinical challenge in that the urologist must balance the threat of progression from non-muscle to muscle invasive disease against the morbidity and mortality of early radical cystectomy (RC) with urinary diversion. Current AUA clinical guidelines for patients with HGT1 disease recommend induction BCG to limit the risk of recurrence and, more importantly, progression after an adequate re-resection (1. Hall MC, Chang SS, Dalbagni G, Pruthi RS, Seigne JD, Skinner EC, et al.: Guideline for the management of nonmuscle invasive bladder cancer (stages Ta, T1, and Tis): 2007 update. J Urol. 2007; 178: 2314-30.). Despite high rates of progression and the associated increase in mortality, the AUA guidelines only state that radical cystectomy as a first-line treatment choice for HGT1 can be considered an option, advising the physician to weigh the likelihood of cure without invasive surgery against the associated morbidity and mortality of radical surgery (1. Hall MC, Chang SS, Dalbagni G, Pruthi RS, Seigne JD, Skinner EC, et al.: Guideline for the management of nonmuscle invasive bladder cancer (stages Ta, T1, and Tis): 2007 update. J Urol. 2007; 178: 2314-30.).

Previous studies have reported that HGT1 bladder cancer will progress to muscle invasive disease in a significant number of patients, making early RC a reasonable course of action to consider (2. Chang SS, Cookson MS: Radical cystectomy for bladder cancer: the case for early intervention. Urol Clin North Am. 2005; 32: 147-55.). In one of the earliest series regarding HGT1 bladder cancer, the authors reported a 53% progression rate at 15 years of follow-up with 34% of patients ultimately dying of urothelial carcinoma (3. Cookson MS, Herr HW, Zhang ZF, Soloway S, Sogani PC, Fair WR: The treated natural history of high risk superficial bladder cancer: 15-year outcome. J Urol. 1997; 158: 62-7.). Other series have demonstrated progression rates ranging from 25 - 56% (4. Shahin O, Thalmann GN, Rentsch C, Mazzucchelli L, Studer UE: A retrospective analysis of 153 patients treated with or without intravesical bacillus Calmette-Guerin forprimary stage T1 grade 3 bladder cancer: recurrence, progression and survival. J Urol. 2003; 169: 96-100; discussion 100.

. Sylvester RJ, van der Meijden AP, Oosterlinck W, Witjes JA, Bouffioux C, Denis L, et al.: Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTCrisk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol. 2006; 49: 466-5; discussion 475-7.

. Herr HW: Tumor progression and survival of patients with high grade, noninvasive papillary (TaG3) bladder tumors:15-year outcome. J Urol. 2000; 163: 60-1; discussion 61-2.
-7. Bol MG, Baak JP, Buhr-Wildhagen S, Kruse AJ, Kjellevold KH, Janssen EA, et al.: Reproducibility and prognostic variability of grade and lamina propria invasion in stages Ta, T1 urothelialcarcinoma of the bladder. J Urol. 2003; 169: 1291-4.).

Understanding the natural history of HGT1 bladder cancer is essential to guiding therapy and creating treatment algorithms that incorporate bladder-sparing protocols along with RC. HGT1 bladder cancer represents a heterogeneous disease with varying phenotypes and outcomes, and currently no test or validated scoring system exists to predict which patients would benefit most from an early RC (8. Stein JP, Penson DF: Invasive T1 bladder cancer: indications and rationale for radical cystectomy. BJU Int. 2008; 102: 270-5.). Thus, this study re-examines the natural history of HGT1 bladder cancer by analyzing the recurrence and progression rates of a large cohort of patients initially diagnosed with HGT1 disease to determine if, in fact, the high incidence of disease progression and death due to bladder cancer is still witnessed in a more contemporary treatment era.

METHODS AND MATERIALS

To identify patients with HGT1 or under the older classification, Grade 3 T1 bladder cancer, two independent databases of non-muscle invasive bladder cancer patients were queried, one at the Atlanta Veteran Affairs Medical Center (AVAMC), the other at the University of Pennsylvania. Institutional Review Board approval was obtained at each institution. Patients identified were diagnosed and treated from 1980 - 2012. Patient demographic, clinical, and pathological variables were examined. Patients were excluded if they had muscle-invasive disease, pure CIS, Ta, or low-grade disease. This produced a total of 222 patients with HGT1 disease to be reviewed, 151 from the University of Pennsylvania database and 71 from the AVAMC.

Biopsies of the bladder distant to the tumor were done at the surgeon’s discretion and pathology was uniformly reported. Tumor characteristics such as tumor size, location, and multifocality were not uniformly reported and therefore were not included in our analysis. Patients were followed with endoscopic surveillance every 3 months for 2 years, 6 months until 5 years, and annually thereafter. Primary outcomes measured were recurrence and progression to muscle invasive disease. Recurrence was defined as any tumor present after initial complete resection at any surveillance point. Stage progression was defined as muscle invasive pathology at any surveillance point. However, patients with MIBC on restaging resection were considered to have MIBC at the time of their initial TUR; they were not considered to represent progression of HGT1 disease and were excluded from the analysis. Data was analyzed with Stata® software and statistics were described with Kaplan Meier curves.

All patients with HGT1 disease were reported in the analysis, including those who received definitive surgery with radical cystectomy prior to the occurrence of muscle invasion. This becomes important during the discussion of these patients being a cohort exposed to a more contemporary treatment era.

RESULTS

A total of 222 patients with HGT1 bladder cancer were identified from the two databases. Patient clinical and demographic data are presented in Table-1. One hundred ninety-eight (89.1%) and 199 (89.6%) of the patients were male and Caucasian, respectively. Mean patient age and pack-years smoking were 66.5 years (range = 29-93 years) and 37.3 (0-125). One hundred ninety-one (86.0%) of the patients presented with isolated high-grade T1 disease, and 31 (14.0%) patients had high-grade T1 disease with concomitant CIS. Two hundred and twelve (95.5%) patients presented with pure urothelial histology while 10 (4.5%) patients had histological variants including micropapillary, sarcomatoid, and squamous differentiation. Peri-operative mitomycin C was used for 41 patients (18.6%); induction BCG was utilized in 175 (78.8%) patients and the mean number of BCG treatments was 5.80 (range = 0-28). One patient received induction mitomycin C (Table-2).

Table 1
Clinical and Demographic Characteristics at Presentation of Patients with High-Grade T1 Bladder Cancer.

Table 2
Recurrence, Progression, and Cause of Death.

At a mean follow-up of 50.8 months (median = 32.5 months, range = 2.2-261.2 months), recurrence occurred in 112 (50.5%) patients. The mean number of recurrences was 1.28 (range = 1-10 recurrences) with a mean and median time to recurrence of 28.8 and 12.9 months, respectively. Progression to muscle-invasive disease occurred in only 19 (8.6%) patients with a mean and median time to progression of 16.6 and 17.2 months. Kaplan Meier curves for recurrence-free and progression-free survival estimates are displayed in Figures 1 and 2.

Figure 1
Kaplan-Meier curve of recurrence free survival.

Figure 2
Kaplan-Meier curve of progression free survival.

At last follow-up, the overall survival of the entire cohort was 76.6%, 170 patients. Only 52 (23.4%) patients had died, 13 (25.0% of deaths, 5.9% of entire cohort) of whose deaths were related to bladder cancer. The remaining 39 deaths (75.0% of deaths, 17.6% of entire cohort) were attributable to patient competing co-morbidities.

DISCUSSION

Consistent with earlier reports demonstrating three to five year progression rates below 10% (9. Herr HW: Restaging transurethral resection of high risk superficial bladder cancer improves the initial response tobacillus Calmette-Guerin therapy. J Urol. 2005; 174: 2134-7.,1010 . Pinsky CM, Camacho FJ, Kerr D, Geller NL, Klein FA, Herr HA, et al.: Intravesical administration of bacillus Calmette-Guérin in patients with recurrent superficial carcinoma of theurinary bladder: report of a prospective, randomized trial. Cancer Treat Rep. 1985; 69: 47-53.), our data shows an 8.6% rate of progression to muscle-invasive disease at a mean follow-up of over four years. This data contrasts the largest prospective studies, which report progression rates of 29% at five years, and 53% at 15 years (3. Cookson MS, Herr HW, Zhang ZF, Soloway S, Sogani PC, Fair WR: The treated natural history of high risk superficial bladder cancer: 15-year outcome. J Urol. 1997; 158: 62-7.,5. Sylvester RJ, van der Meijden AP, Oosterlinck W, Witjes JA, Bouffioux C, Denis L, et al.: Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTCrisk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol. 2006; 49: 466-5; discussion 475-7.). Notably, a majority of the patients who progressed in our study presented with variant histology. Additionally, in our large contemporary cohort, 13 patients (5.9%) died due to bladder cancer. This present data may argue for a more conservative approach for patients with HGT1 disease in the absence of high-risk features for progression such as variant histology and CIS.

The high rates of progression and mortality seen in past studies have spurred clinicians to advocate early definitive, radical surgery for patients with HGT1 disease, particularly if they have certain high-risk features (2. Chang SS, Cookson MS: Radical cystectomy for bladder cancer: the case for early intervention. Urol Clin North Am. 2005; 32: 147-55.,8. Stein JP, Penson DF: Invasive T1 bladder cancer: indications and rationale for radical cystectomy. BJU Int. 2008; 102: 270-5.,1111 . Nieder AM, Brausi M, Lamm D, O’Donnell M, Tomita K, Woo H, et al.: Management of stage T1 tumors of the bladder: International Consensus Panel. Urology. 2005; 66: 108-25.,1212 . Kulkarni GS, Hakenberg OW, Gschwend JE, Thalmann G, Kassouf W, Kamat A, et al.: An updated critical analysis of the treatment strategy for newly diagnosed high-grade T1 (previously T1G3)bladder cancer. Eur Urol. 2010; 57: 60-70.). Despite no randomized trials, multiple retrospective studies have shown advantages for disease-specific and overall survivals in patients treated with RC before muscle invasion occurs (1313 . Herr HW, Sogani PC: Does early cystectomy improve the survival of patients with high risk superficial bladder tumors? J Urol. 2001; 166: 1296-9.

14 . Sternberg IA, Keren Paz GE, Chen LY, Herr HW, Dalbagni G: Role of immediate radical cystectomy in the treatment of patients with residual T1 bladder cancer onrestaging transurethral resection. BJU Int. 2013; 112: 54-9.

15 . Raj GV, Herr H, Serio AM, Donat SM, Bochner BH, Vickers AJ, et al.: Treatment paradigm shift may improve survival of patients with high risk superficial bladder cancer. J Urol. 2007; 177: 1283-6; discussion 1286.
-1616 . Denzinger S, Fritsche HM, Otto W, Blana A, Wieland WF, Burger M: Early versus deferred cystectomy for initial high-risk pT1G3 urothelial carcinoma of the bladder: do riskfactors define feasibility of bladder-sparing approach? Eur Urol. 2008; 53: 146-52.). In these series, reasons to advocate for early RC include residual T1 disease at re-staging resection, extensive multifocal disease, large tumor volume, location making endoscopic management difficult, variant histology, and presence of CIS (2. Chang SS, Cookson MS: Radical cystectomy for bladder cancer: the case for early intervention. Urol Clin North Am. 2005; 32: 147-55.,5. Sylvester RJ, van der Meijden AP, Oosterlinck W, Witjes JA, Bouffioux C, Denis L, et al.: Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTCrisk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol. 2006; 49: 466-5; discussion 475-7.,1111 . Nieder AM, Brausi M, Lamm D, O’Donnell M, Tomita K, Woo H, et al.: Management of stage T1 tumors of the bladder: International Consensus Panel. Urology. 2005; 66: 108-25.

12 . Kulkarni GS, Hakenberg OW, Gschwend JE, Thalmann G, Kassouf W, Kamat A, et al.: An updated critical analysis of the treatment strategy for newly diagnosed high-grade T1 (previously T1G3)bladder cancer. Eur Urol. 2010; 57: 60-70.
-1313 . Herr HW, Sogani PC: Does early cystectomy improve the survival of patients with high risk superficial bladder tumors? J Urol. 2001; 166: 1296-9.,1717 . Bianco FJ Jr, Justa D, Grignon DJ, Sakr WA, Pontes JE, Wood DP Jr.: Management of clinical T1 bladder transitional cell carcinoma by radical cystectomy. Urol Oncol. 2004; 22: 290-4.,1818 . Herr HW, Donat SM, Dalbagni G: Can restaging transurethral resection of T1 bladder cancer select patients for immediate cystectomy? J Urol. 2007; 177: 75-9; discussion 79.). Nevertheless, it is important to note that in these prior series, clinical understaging was prevalent in these patients treated with early RC (1313 . Herr HW, Sogani PC: Does early cystectomy improve the survival of patients with high risk superficial bladder tumors? J Urol. 2001; 166: 1296-9.,1717 . Bianco FJ Jr, Justa D, Grignon DJ, Sakr WA, Pontes JE, Wood DP Jr.: Management of clinical T1 bladder transitional cell carcinoma by radical cystectomy. Urol Oncol. 2004; 22: 290-4.), indicating, perhaps, that a portion of the survival benefit seen in patients undergoing early cystectomy is really a function of a poor clinical staging of bladder cancer.

To appreciate the lower progression rate seen in our series, the patient cohort must be viewed in the context of contemporary developments in the management of HGT1 bladder cancer. Increasingly, clinicians routinely perform a restaging TUR for patients with HGT1 bladder cancer followed by induction and maintenance BCG (1. Hall MC, Chang SS, Dalbagni G, Pruthi RS, Seigne JD, Skinner EC, et al.: Guideline for the management of nonmuscle invasive bladder cancer (stages Ta, T1, and Tis): 2007 update. J Urol. 2007; 178: 2314-30.). High incidences of clinical understaging (34 - 64%) have been cited to support this recommendation (1111 . Nieder AM, Brausi M, Lamm D, O’Donnell M, Tomita K, Woo H, et al.: Management of stage T1 tumors of the bladder: International Consensus Panel. Urology. 2005; 66: 108-25.,1919 . 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 anemphasis on the inadequacy of the tumor, nodes and metastases classification. J Urol. 1991; 145: 45-50.

20 . Freeman JA, Esrig D, Stein JP, Simoneau AR, Skinner EC, Chen SC, et al.: Radical cystectomy for high risk patients with superficial bladder cancer in the era of orthotopic urinaryreconstruction. Cancer. 1995; 76: 833-9.

21 . Dutta SC, Smith JA Jr, Shappell SB, Coffey CS, Chang SS, Cookson MS: Clinical under staging of high risk nonmuscle invasive urothelial carcinoma treated with radicalcystectomy. J Urol. 2001; 166: 490-3.
-2222 . Herr HW: The value of a second transurethral resection in evaluating patients with bladder tumors. J Urol. 1999; 162: 74-6.). Restaging TUR and identification of patients with clinical T2 disease that should be treated with RC shows a substantial advantage for recurrence and progression free survival (2323 . Herr HW: Role of re-resection in non-muscle-invasive bladder cancer. ScientificWorldJournal. 2011; 11: 283-8.). Furthermore, restaging TUR before BCG has been shown to improve the response to the intravesical immunotherapy, lowering the observed recurrence and progression rates from 57% and 34% to 29% and 7%, respectively, at 3 year follow-up (9. Herr HW: Restaging transurethral resection of high risk superficial bladder cancer improves the initial response tobacillus Calmette-Guerin therapy. J Urol. 2005; 174: 2134-7.). Thus, the routine use of restaging TUR has two effects on the progression rate of patients with HGT1 disease: first, it selects out patients with clinical T2 disease, removing them from the HGT1 cohort and improving the measured progression rate. Secondly, restaging TUR should resect all remaining visible tumor and thereby improve the response to BCG therapy, further improving the progression rate for patients with HGT1 disease.

Our contemporary cohort also likely benefited from more sophisticated pathologic examinations as histologic variants with more aggressive phenotypes requiring more aggressive treatment have become recognized (2424 . Shah RB, Montgomery JS, Montie JE, Kunju LP: Variant (divergent) histologic differentiation in urothelial carcinoma is under-recognized in communitypractice: impact of mandatory central pathology review at a large referral hospital. Urol Oncol. 2013; 31: 1650-5.). For example, the presence of micropapillary histology, in particular, has been shown to be a poor prognostic factor for progression and disease free survival, and these patients deserve consideration for RC before muscle invasive disease occurs (2525 . Kamat AM, Dinney CP, Gee JR, Grossman HB, Siefker-Radtke AO, Tamboli P, et al.: Micropapillary bladder cancer: a review of the University of Texas M. D. Anderson Cancer Centerexperience with 100 consecutive patients. Cancer. 2007; 110: 62-7.). The high incidence of these variant histologies was established with a recent large series showing variant histology was present in 19.9% of transurethral biopsies (2424 . Shah RB, Montgomery JS, Montie JE, Kunju LP: Variant (divergent) histologic differentiation in urothelial carcinoma is under-recognized in communitypractice: impact of mandatory central pathology review at a large referral hospital. Urol Oncol. 2013; 31: 1650-5.). It appears that these aggressive variant histologies are being identified more routinely, and patients are now more likely to be offered early RC and less likely to be managed with bladder sparing therapy, potentially improving progression rates.

This study has a number of limitations. It is a retrospective review open to significant selection bias. As previously discussed, restaging TUR, recognition of histologic variants, and an increased willingness of clinicians to manage worrisome high-risk patients with RC distorts this patient cohort and potentially makes it more an analysis of low-risk HGT1 patients. Importantly, this analysis was done with a relatively short follow up time compared to the prior report that established the natural history of HGT1 bladder cancer (3. Cookson MS, Herr HW, Zhang ZF, Soloway S, Sogani PC, Fair WR: The treated natural history of high risk superficial bladder cancer: 15-year outcome. J Urol. 1997; 158: 62-7.). At further follow-up, our reported progression rates may increase, nullifying these promising rates of prevention of progression to muscle-invasive disease. Furthermore, there are many tumor factors with important prognostic implications that are not accounted for in this study, making it difficult to characterize and compare the biology of this cohort with previous cohorts. Additionally, as restaging TUR has only recently become routine, our databases poorly captured which patients received this procedure, introducing uncertainty in the analysis of progression versus inadequate primary resection. Moreover, our database poorly captured which patients were treated with radical cystectomy, the time of surgical intervention, and also does not contain the pathologic outcomes of these surgeries.

Nevertheless, it is important to contextualize these results in that many patients diagnosed with HGT1 bladder cancer do not have a 15-year life expectancy. Thus, it is imperative to weigh the expected risk of disease progression against the morbidity and mortality of surgery in the context of a patient’s life expectancy, considering one’s co-morbidities and goals of care.

CONCLUSIONS

At approximately 4 years of follow-up, the progression rate to muscle-invasive disease in patients initially presenting with high-grade T1 bladder cancer is only 8.6%. Although potentially subject to selection biases, these results from a large, contemporary patient cohort appears promising, arguing against the routine use of early cystectomy. Clearly further follow-up is needed, however when one considers the potential morbidity and mortality of radical cystectomy, the progression rate reported here is acceptable, especially when risk-stratified against an older and co-morbid individual.

REFERENCES

  • 1
    Hall MC, Chang SS, Dalbagni G, Pruthi RS, Seigne JD, Skinner EC, et al.: Guideline for the management of nonmuscle invasive bladder cancer (stages Ta, T1, and Tis): 2007 update. J Urol. 2007; 178: 2314-30.
  • 2
    Chang SS, Cookson MS: Radical cystectomy for bladder cancer: the case for early intervention. Urol Clin North Am. 2005; 32: 147-55.
  • 3
    Cookson MS, Herr HW, Zhang ZF, Soloway S, Sogani PC, Fair WR: The treated natural history of high risk superficial bladder cancer: 15-year outcome. J Urol. 1997; 158: 62-7.
  • 4
    Shahin O, Thalmann GN, Rentsch C, Mazzucchelli L, Studer UE: A retrospective analysis of 153 patients treated with or without intravesical bacillus Calmette-Guerin forprimary stage T1 grade 3 bladder cancer: recurrence, progression and survival. J Urol. 2003; 169: 96-100; discussion 100.
  • 5
    Sylvester RJ, van der Meijden AP, Oosterlinck W, Witjes JA, Bouffioux C, Denis L, et al.: Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTCrisk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol. 2006; 49: 466-5; discussion 475-7.
  • 6
    Herr HW: Tumor progression and survival of patients with high grade, noninvasive papillary (TaG3) bladder tumors:15-year outcome. J Urol. 2000; 163: 60-1; discussion 61-2.
  • 7
    Bol MG, Baak JP, Buhr-Wildhagen S, Kruse AJ, Kjellevold KH, Janssen EA, et al.: Reproducibility and prognostic variability of grade and lamina propria invasion in stages Ta, T1 urothelialcarcinoma of the bladder. J Urol. 2003; 169: 1291-4.
  • 8
    Stein JP, Penson DF: Invasive T1 bladder cancer: indications and rationale for radical cystectomy. BJU Int. 2008; 102: 270-5.
  • 9
    Herr HW: Restaging transurethral resection of high risk superficial bladder cancer improves the initial response tobacillus Calmette-Guerin therapy. J Urol. 2005; 174: 2134-7.
  • 10
    Pinsky CM, Camacho FJ, Kerr D, Geller NL, Klein FA, Herr HA, et al.: Intravesical administration of bacillus Calmette-Guérin in patients with recurrent superficial carcinoma of theurinary bladder: report of a prospective, randomized trial. Cancer Treat Rep. 1985; 69: 47-53.
  • 11
    Nieder AM, Brausi M, Lamm D, O’Donnell M, Tomita K, Woo H, et al.: Management of stage T1 tumors of the bladder: International Consensus Panel. Urology. 2005; 66: 108-25.
  • 12
    Kulkarni GS, Hakenberg OW, Gschwend JE, Thalmann G, Kassouf W, Kamat A, et al.: An updated critical analysis of the treatment strategy for newly diagnosed high-grade T1 (previously T1G3)bladder cancer. Eur Urol. 2010; 57: 60-70.
  • 13
    Herr HW, Sogani PC: Does early cystectomy improve the survival of patients with high risk superficial bladder tumors? J Urol. 2001; 166: 1296-9.
  • 14
    Sternberg IA, Keren Paz GE, Chen LY, Herr HW, Dalbagni G: Role of immediate radical cystectomy in the treatment of patients with residual T1 bladder cancer onrestaging transurethral resection. BJU Int. 2013; 112: 54-9.
  • 15
    Raj GV, Herr H, Serio AM, Donat SM, Bochner BH, Vickers AJ, et al.: Treatment paradigm shift may improve survival of patients with high risk superficial bladder cancer. J Urol. 2007; 177: 1283-6; discussion 1286.
  • 16
    Denzinger S, Fritsche HM, Otto W, Blana A, Wieland WF, Burger M: Early versus deferred cystectomy for initial high-risk pT1G3 urothelial carcinoma of the bladder: do riskfactors define feasibility of bladder-sparing approach? Eur Urol. 2008; 53: 146-52.
  • 17
    Bianco FJ Jr, Justa D, Grignon DJ, Sakr WA, Pontes JE, Wood DP Jr.: Management of clinical T1 bladder transitional cell carcinoma by radical cystectomy. Urol Oncol. 2004; 22: 290-4.
  • 18
    Herr HW, Donat SM, Dalbagni G: Can restaging transurethral resection of T1 bladder cancer select patients for immediate cystectomy? J Urol. 2007; 177: 75-9; discussion 79.
  • 19
    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 anemphasis on the inadequacy of the tumor, nodes and metastases classification. J Urol. 1991; 145: 45-50.
  • 20
    Freeman JA, Esrig D, Stein JP, Simoneau AR, Skinner EC, Chen SC, et al.: Radical cystectomy for high risk patients with superficial bladder cancer in the era of orthotopic urinaryreconstruction. Cancer. 1995; 76: 833-9.
  • 21
    Dutta SC, Smith JA Jr, Shappell SB, Coffey CS, Chang SS, Cookson MS: Clinical under staging of high risk nonmuscle invasive urothelial carcinoma treated with radicalcystectomy. J Urol. 2001; 166: 490-3.
  • 22
    Herr HW: The value of a second transurethral resection in evaluating patients with bladder tumors. J Urol. 1999; 162: 74-6.
  • 23
    Herr HW: Role of re-resection in non-muscle-invasive bladder cancer. ScientificWorldJournal. 2011; 11: 283-8.
  • 24
    Shah RB, Montgomery JS, Montie JE, Kunju LP: Variant (divergent) histologic differentiation in urothelial carcinoma is under-recognized in communitypractice: impact of mandatory central pathology review at a large referral hospital. Urol Oncol. 2013; 31: 1650-5.
  • 25
    Kamat AM, Dinney CP, Gee JR, Grossman HB, Siefker-Radtke AO, Tamboli P, et al.: Micropapillary bladder cancer: a review of the University of Texas M. D. Anderson Cancer Centerexperience with 100 consecutive patients. Cancer. 2007; 110: 62-7.
  • ABBREVIATIONS
    HGT1 = High-grade T1
    NMIBC = Non-muscle invasive bladder cancer
    AVAMC = Atlanta Veterans’ Administration Medical Center
    CIS = Carcinoma in situ
    BCG = Bacillus Calmette-Guerin
    RC = Radical cystectomy
    TUR = Transurethral resection

Publication Dates

  • Publication in this collection
    Mar-Apr 2014

History

  • Received
    26 Oct 2013
  • Accepted
    12 Feb 2014
Sociedade Brasileira de Urologia Rua Bambina, 153, 22251-050 Rio de Janeiro RJ Brazil, Tel. +55 21 2539-6787, Fax: +55 21 2246-4088 - Rio de Janeiro - RJ - Brazil
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