Follow-up After Surgical Treatment of Bladder Cancer: A Critical Analysis of the Literature

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1 EUROPEAN UROLOGY 62 (2012) available at journal homepage: ollaborative Review Urothelial ancer Follow-up After Surgical Treatment of Bladder ancer: A ritical Analysis of the Literature Viktor Soukup a, *, Marko Babjuk b, Joaquim Bellmunt c, Guido Dalbagni d, Gianluca Giannarini e, Oliver W. Hakenberg f, Harry Herr d, Eric Lechevallier g, Maria J. Ribal h a Department of Urology, General Teaching Hospital and 1st Faculty of Medicine, harles University in Praha, Praha, zech Republic; b Department of Urology, Hospital in Motol and 2nd Faculty of Medicine, harles University in Praha, Praha, zech Republic; c Medical Oncology Service, University Hospital del Mar, Barcelona, Spain; d Department of Urology, Memorial Sloan-Kettering ancer entre, New York, NY, USA; e Department of Urology, University of Berne, Inselspital, Berne, Switzerland; f Department of Urology, Rostock University, Rostock, Germany; g Hôpital la onception, Marseille, France; h Department of Urology, Hospital linic-university of Barcelona, Barcelona, Spain Article info Article history: Accepted May 3, 2012 Published online ahead of print on May 11, 2012 Keywords: ystoscopy Follow-up Muscle-invasive bladder cancer Non muscle-invasive bladder cancer Progression Radical cystectomy Recurrence Abstract ontext: Follow-up of patients treated for bladder cancer (Ba) is of great importance for both non muscle-invasive Ba (NMIB) and muscle-invasive Ba (MIB) because of the high incidence of recurrence and progression. The schedule and methods of followup should reflect the individual clinical situation. Objective: To evaluate the existing evidence for intensity and duration of follow-up recommendations in patients after surgical treatment of Ba. Evidence acquisition: We searched the Medline, Embase, and ochrane databases for published data on the follow-up of patients with NMIB and MIB after radical cystectomy (R). Evidence synthesis: Follow-up in patients with NMIB is necessary because of the high probability of tumour recurrence and the risk of progression. ystoscopy plus cytology are the standard methods for follow-up. ystoscopy should be done 3 mo after the transurethral resection in every patient, and the frequency after that depends on the individual recurrence/progression risk. ytology should be used as an adjunctive method to cystoscopy in intermediate- and high-risk patients. None of the currently available urinary markers or imaging methods can substitute for cystoscopy-based follow-up. High-risk NMIB patients require regular lifelong upper urinary tract monitoring. Follow-up in MIB is based on the fact that early detection of recurrence after R allows for timely treatment with the aim of improving outcomes. Patients with extravesical and lymph node positive disease should have the most intensive follow-up because of the highest recurrence risk. Routine upper urinary tract imaging is advisable for all patients and should continue in the long term. Follow-up also allows for early detection of urinary diversion related complications, the rate of which increases with time. onclusions: Follow-up in Ba is necessary for diagnosing recurrence and progression, as well as for evaluating complications after radical treatment. Since randomised studies investigating the most appropriate follow-up schedule are lacking, most recommendations are based on only the retrospective experience. Nonetheless, reasonable recommendations can be made until further prospective randomised studies testing different follow-up schedules have been performed. # 2012 European Association of Urology. Published by Elsevier B.V. All rights reserved. * orresponding author. Department ofurology, General TeachingHospital and1stfaculty of Medicine, harles University in Praha, Ke Karlovu 6, Praha 2, 12808, zech Republic. Tel address: viktor.soukup@seznam.cz (V. Soukup) /$ see back matter # 2012 European Association of Urology. Published by Elsevier B.V. All rights reserved.

2 EUROPEAN UROLOGY 62 (2012) Introduction Follow-up of patients treated for bladder cancer (Ba) is of great importance for both non muscle-invasive Ba (NMIB) and muscle-invasive Ba (MIB) because of the high incidence of recurrence and progression after both transurethral resection [1 4] and radical cystectomy (R) [5]. The schedule and methods of follow-up, however, should reflect the individual clinical situation. In this review, we aim to evaluate the existing evidence for the timing and extent of follow-up in patients after surgical treatment of Ba and to provide recommendations for practicing urologists. 2. Evidence acquisition We performed a systematic search of the Medline, Embase, and ochrane databases up to December The Medical Subject Heading terms carcinoma, transitional cell, urinary bladder, urinary bladder neoplasms, follow-up, and surveillance were used. Search limits were Human/English language/randomised controlled trials/linical trials/ Review articles/meta-analysis/practice guidelines. We retrieved and evaluated all relevant articles published between 1995 and Older studies were included selectively if historically relevant or, in the case of scanty data, in more recent publications. All authors screened the abstracts retrieved by the search, and a final consensus on all publications included in the present review was obtained. The level of evidence (LE) and grade of recommendation (GR) were provided with use of the modified Oxford entre for Evidence Based Medicine scheme [6]. 3. Evidence synthesis There are very few studies that are primarily focused on follow-up scheme, methods and tests used during followup, and trying to define the best follow-up practice. Most studies available are nonexperimental, and the data presented are level 3 and, less frequently, level 2b evidence Follow-up of non muscle-invasive bladder cancer Rationale The schedule and methods of follow-up should reflect the individual risk of recurrence and progression [1,4]. The early detection of muscle-invasive and high-grade recurrence is critical, as this scenario can be life-threatening. In contrast, small low-grade recurrences do not pose a threat, and early detection is not essential Risk stratification The risk of recurrence and progression in NMIB depends on several clinical and histologic parameters. The European Organisation for Research and Treatment of ancer (EORT) provided a scoring system and risk tables for the prediction of short- and long-term risks of both recurrence and progression. The EORT scoring system is based on six factors (number of tumours, tumour size, prior recurrence status, T stage, presence of concomitant carcinoma in situ [IS], and grade) [2]. The limitation of the model is that the EORT evaluation was based on studies that included mainly patients without routine repeated transurethral resection of the bladder (re-turb), without immediate/ early instillation treatment and without maintenance bacillus almette-guérin (BG) treatment. Thus, the EORT tables tend to overestimate the risk of recurrence and progression [7]. A scoring model for BG-treated patients has been developed by the lub Urológico Español De Tratamiento Oncológico (UETO) [3]. The model is based on seven factors: gender, age, prior recurrence status, number of tumours, T stage category, associated IS, and grade. In the UETO score, the calculated risk of recurrence and progression in high-risk patients is lower than that risk obtained with EORT tables and may be explained by the inclusion of studies using BG treatment in the UETO analysis. Both the EORT and the UETO scores, however, are a good basis for estimating the need and timing of follow-up after transurethral resection of the bladder (TURB) for NMIB. Nevertheless, external validations of both systems are still needed ystoscopy Follow-up in NMIB primarily depends on the cystoscopic inspection of the whole bladder. Although time-consuming and invasive, cystoscopies are essential, and the question is how often and how long they should be performed First follow-up cystoscopy. The first cystoscopy after complete TURB of the NMIB is of great importance, as it has prognostic value (Table 1). There are no data that define an optimal timing for this first follow-up cystoscopy. The European Association of Urology (EAU) guidelines suggest a 3-mo interval [1]. However, in Sweden, the first follow-up cystoscopy is usually performed after 4 mo [8]; similarly, in some regions of the United Kingdom, the procedure is performed between 3 and 4 mo after the TURB in 84 88% of cases [9]. It has been shown that early tumour recurrence at 3 mo can be detected in a significant number of patients (Table 1). However, the rate of recurrence at 3 mo will also depend on the completeness of the initial TURB, whether or not a routine re-turb has been done, and the intravesical treatment administered. In the combined analysis of seven EORT randomised trials (without re-turb), early tumour recurrence was observed in 13.1% (6.7 40%) of 2410 patients (LE 2b) [10]; clearly, this finding will also include tumour persistence in a considerable percentage of cases. Several analyses suggest that the result of the first follow-up cystoscopy provides important prognostic information irrespective of the risk group and previous intravesical treatment (LE 1a) [2,8,11 17] (Table 1) Schedule of further cystoscopies. When the first followup cystoscopy 3 mo after TURB is negative, the next cystoscopies are traditionally repeated every 3 mo for a

3 292 Table 1 Prognostic value of the first follow-up cystoscopy Author Year Patients, no. Patient characteristics Time to first cystoscopy Positive first cystoscopy, % Prognostic value omment Fitzpatrick et al. [24] TaG1 2 3 mo 46.9 Not assessed Patient with no recurrence at 3 mo had 80% chance of having no further recurrence; patient with recurrence at 3 mo, only 10% Parmar et al. [13] TaT1, G1 3, some of them intravesical thiotepa 3 mo 33 Result of 3-mo cystoscopy was the single most important factor for recurrence on multivariate analysis 2-yr recurrence-free rates: 66% and 30% in patients with negative and positive 3-mo cystoscopy Herr et al. [14] TaT1is, BG treated 3 mo 8.7 Predictor of progression 82% of T1 tumours at 3-mo cystoscopy developed subsequent progression Kurth et al. [12] TaT1, G1 3, all treated with intravesical chemotherapy Oge et al. [15] TaG1, G2, <4 cm, without intravesical therapy Solsona et al. [16] T1G3 or associated IS, intravesical treatment (BG or MM) 3 mo 17 Most important prognostic factor for the long-term recurrence rate 3 mo 6.5 No prognostic value for the following first-year controls 3 mo 21.5 Predictor of progression in multivariate analysis Holmang et al. [8] Ta, T1, PUNLMP, G d 40.6 First cystoscopy finding independent predictor of recurrence and progression on multivariate analysis Sylvester et al. [2] Ta, T1, is, G1 3, 78% with intravesical treatment, only one study with induction course of BG Fernandez-Gomez et al. [11] 3 mo 12.1 Significant prognostic importance on the time to progression Ta, T1, is, G1 3, BG treated 3 mo NA Independent progression predictor in multivariate analysis Palou et al. [17] T1G2 (17% chemotherapy, 5% BG) 3 mo 6.7 Predictor of progression in multivariate analysis Patient with no recurrence at 3 mo had 53% chance of having no further recurrence; patient with recurrence at 3 mo, only 17% Progression in 80.4% of patients with positive 3-mo cystoscopy In patients with PUNLMP or WHO grade 1 and pta tumours, mean time to subsequent recurrence: 20 mo Progression in 25.6% of patients with positive 3-mo cystoscopy and in 8.7% with negative 3-mo cystoscopy No role in prediction of further recurrence EUROPEAN UROLOGY 62 (2012) BG = bacillus almette-guérin; IS = carcinoma in situ; MM = mitomycin ; PUNLMP = papillary urothelial neoplasm of low malignant potential; WHO = World Health Organisation; NA = not available.

4 EUROPEAN UROLOGY 62 (2012) period of 2 yr, then every 6 mo until the end of the fifth year, and yearly thereafter. This approach has now been tailored to the individual risk, which, according to the EAU guidelines, should be assessed following the EORT score [1]. Thus, the traditional intensive schedule is now recommended only for high-risk patients, whereas a reduced frequency of cystoscopies is appropriate for lowand intermediate-risk groups. This grade recommendation of the EAU guidelines, however, reflects the low level of evidence supporting this statement [1]. The American Urological Association (AUA) guidelines recommend a risk-adapted approach, with more intensive follow-up for high-risk patients as well [4]. However, a survey of clinical practice in The Netherlands and Belgium reported that most urologists adhere to a schedule of four cystoscopies during the first year for lowrisk tumours as well [18]. This practice may be attributed to the fact that risk adaptation in follow-up for NMIB has only fairly recently been introduced into guideline recommendations. However, data from the United States also show very low compliance with guideline recommendations for follow-up cystoscopies; up to 42% of physicians have not performed at least one cystoscopy or one cytology for a single patient nested within their practice during the initial 2 yr after diagnosis of high-risk NMIB (LE 2b) [19]. It can be safely surmised that an extensive traditional and rigid schedule for follow-up cystoscopies is not needed for all patients. In 1995, Olsen and Genster demonstrated in 97 randomised patients with TaG1/2 tumours that the interval between cystoscopies can be safely doubled (LE 1b) [20]. Based on such data, if the first cystoscopy after 3 mo is negative in low-risk tumours, it seems safe to perform the next follow-up cystoscopy 9 mo later (LE 4) [21]. For the further schedule, a risk-adapted approach is recommended (GR ) an patients be discharged from cystoscopic follow-up?. It is generally accepted that patients with high-risk NMIB need long-term follow-up. Recent data support the need for longterm follow-up of >10 15 yr in such patients even after initial response to BG therapy and a recurrence-free period >5 yr (LE 3) [22]. Although the available data are conflicting, patients with low-risk NMIB probably do not need lifelong follow-up. Of 115 patients with TaG1 NMIB who did not have a recurrence in 5 yr, 98.3% remained tumour-free for 20 yr (LE 3) [23]. In another study with TaG1 2 NMIB patients who remained free of recurrence for 5 yr after TURB, there was a 92% chance of having no further recurrence at all (LE 3) [24]. Holmäng et al. reported only 2 of 59 patients with a recurrence after a recurrence-free interval of 5 yr (LE 3) [25]. In a cohort of 179 patients with Ta/T1 tumours, the probability of a patient s developing a recurrence after being tumour-free for 2, 5, and 10 yr was 43%, 22%, and 2%, respectively. In this study, no patient had a recurrence after remaining tumour-free for 12 yr (LE 3) [26]. However, long-term recurrences, even in low-risk tumours, do occur. Leblanc et al. reported that 14% of recurrences were detected >5 yr after the first diagnosis of TaG1 tumours (LE 3) [27]. The reported 2-, 5-, and 10-yr recurrence-free rates in 53 patients with papillary urothelial neoplasm of low malignant potential and a median follow-up of 11.7 yr were 66%, 51%, and 36%, respectively. No patient developed high-grade tumours, MIB, or upper urinary tract tumours (UUTTs), but there still was a high and long-term risk of recurrence (LE 3) [28]. Thus, although the risk of recurrence in low-risk patients after 5 recurrencefree years does not seem to be nonexistent, it is very low, and regular cystoscopic follow-up can be discontinued [1,29]. An alternative, less invasive method of assessment, such as bladder ultrasonography, may be considered (GR ) How can the diagnostic performance of surveillance cystoscopy be improved? ystoscopy remains the standard of diagnosis, but the procedure is invasive, costly, and labourious, and it has some limitations in the detection of flat and very small papillary lesions. An increase in the sensitivity of surveillance cystoscopy could allow for a decrease in the total number of cystoscopies performed. Both fluorescence cystoscopy (F) and narrow-band imaging (NBI) are reported to have better sensitivities but lower specificities than white light cystoscopy in the detection of Ba (LE 2a) [30,31]. Most studies performed, however, employed F and NBI as a part of TURB, and fewer studies used these applications with flexible instruments for follow-up cystoscopy. Superior results in the detection of small papillary and flat lesions compared with white light cystoscopy have been reported (LE 2a) [32,33], but whether this reported better detection can safely be relied on to prolong the intervals for surveillance cystoscopies is unknown. Other new optical diagnostic cystoscopic tools, such as Raman spectroscopy and optical coherence tomography, cannot yet be applied as routine surveillance examination [34]. If urine-based tests (cytology, markers) are used as an adjunct to surveillance cystoscopy, the accuracy of cystoscopy can be increased by the knowledge of urine test outcome because of a diagnostic review bias. The awareness of a positive urine test result may significantly improve the cystoscopic detection rate (LE 1b) [35] When are bladder biopsies necessary during follow-up? Endoscopy under anaesthesia and bladder biopsies should be performed when office cystoscopy shows suspicious findings or if urinary cytology is positive. Some authors recommend endoscopy under anaesthesia with biopsies for all patients after initial BG treatment, because the frequent erythematous findings in these patients cannot be distinguished from IS without histology [36]. Dalbagni et al, however, reported that biopsy could be omitted in patients with normal office cystoscopy and in those with erythematous findings if urine cytology is normal (LE 2b) [37] Urinary markers Urinary markers might be used for monitoring patients during follow-up as a less invasive method with perhaps lower costs. There are currently two clinical objectives of

5 294 EUROPEAN UROLOGY 62 (2012) marker application in the follow-up of NMIB: (1) as an adjunct to cystoscopy with the objective of improving the detection of IS and reducing the false-negative rate (a good marker should have high sensitivity for high-grade tumours and high specificity) and (2) as a substitute for some cystoscopies during follow-up (a marker should have high sensitivity, particularly for high-grade tumours). An ideal marker is one that can achieve the same or higher accuracy of cystoscopy and cytology together, but such a marker currently is not available. Another important aspect is the patient s opinion and the patient s need for a reliable diagnosis. If the sensitivity of a urinary test is <90 95%, most patients prefer flexible cystoscopy with a definitive diagnosis for follow-up (LE 3) [38]. As yet, none of the available urine markers fulfils these criteria. Thus, at present, no urine marker can safely replace cystoscopy during follow-up (GR A) [1,39] ell-based urinary diagnosis: cytology, fluorescence in situ hybridisation. Urinary cytology is the standard urine test in routine clinical use. It is used in conjunction with follow-up cystoscopy to detect disease that may be missed by routine cystoscopy (IS, upper tract disease, prostatic urethra involvement). Voided urine cytology is highly tumourspecific and has a good sensitivity to detect high-grade tumours. In the study by Mowatt et al. (LE 2b) [30] including participants, the pooled sensitivity and specificity of cytology were 44% and 96%, respectively. The median sensitivity of cytology was 27% in patients with low-risk tumours (pta, G1/2), 69% in patients with high-risk tumours (T1G3), and 78% in patients with IS. Shortcomings of urinary cytology are its low sensitivity in low-risk tumours and its interobserver variability. onsequently, the AUA guidelines recommend cytology for follow-up in patients with high-risk tumours [4]; the EAU guidelines recommend it for patients with high- and intermediate-risk tumours [1] (GR ). Fluorescence in situ hybridisation (FISH) has a reported sensitivity of 64% and a specificity of 73% in patients with a history of NMIB (LE 2b) [30]. FISH should be unaffected by BG treatment, and patients with a positive post-bg result were reported to be more likely to relapse (2.7-fold greater risk) (LE 2b) [40]. However, there are also no data supporting the use of FISH instead of cystoscopy in NMIB surveillance Soluble urine markers. The use of single urinary markers has not added much to urine examination by cytology. Almost all markers tested in follow-up of patients with NMIB have a higher sensitivity but a lower specificity than urine cytology (Table 2) [41 43]. An analysis combining a panel of markers spanning different pathways seems to be the better approach. In such marker panels, a higher sensitivity but lower specificity was described compared with the use of a single urine marker (LE 2b) [44,45]. Marker-guided follow-up, especially of patients with lowrisk NMIB, appears attractive; however, based upon the current level of evidence, this procedure cannot be recommended at present (GR B). Table 2 Sensitivity and specificity of urinary markers in the detection of non muscle-invasive bladder cancer recurrence Marker Sensitivity, % Specificity, % ytology [29] FISH [29] 64 (median) 73 (median) Immunocyte [29] 81 (median) 75 (median) Telomerase [42] NA BTA-Trak [42] BTA-stat [42] NMP22 [29] MSA [41] YFRA 21 1 [42] Ubiquitin [42] FISH = fluorescence in situ hybridization; NA = not available; NMP22 = nuclear matrix protein 22; MSA = microsatellite analysis Imaging in the follow-up of non muscle-invasive bladder cancer Imaging of the urinary bladder. Transabdominal sonography has low sensitivity in detecting small bladder tumours [46]; despite recent promising results reporting 78.5% sensitivity and 100% specificity for modern ultrasonographic techniques (LE 3) [47], the procedure cannot be recommended to replace cystoscopy as a follow-up tool for NMBI (GR B). A precise role for multidetector computed tomography (T) in Ba patients has not been established. T has reported sensitivities in the range of 79 90% and specificities in the range of 91 95% (LE 2b) [46]. The accuracy of T urography is lower in patients with a recurrent tumour, because it is difficult to distinguish recurrence from changes resulting from TURB. Also, tumour at the bladder base can be missed, and flat tumours do not appear as a filling defect. The sensitivity of T urography is not as high as that of cystoscopy [46]. Virtual T cystoscopy has a reported sensitivity comparable to T urography and higher than virtual magnetic resonance imaging (MRI) cystoscopy or virtual ultrasonographic cystoscopy (LE 2b) [48]. None of these imaging methods has enough sensitivity to replace cystoscopy in the follow-up of patients with NMIB (GR ) Upper urinary tract evaluation. The risk factors for the development of UUTTs in patients with NMIB are tumour multiplicity, tumour in the trigone, bladder IS, tumour grade, stage, and vesicoureteral reflux [49,50]. In patients with a history of NMIB, the risk of recurrence in the upper urinary tract significantly differs between theriskgroups.inthestudybymillán-rodríguez et al., 1529 patients were followed for a mean of 4.2 yr. In the low-, intermediate-, and high-risk Ba group, the incidence of UUTT was 0.6%, 1.8%, and 4.1%, respectively (LE 3) [49]. In another study by Hurle et al, after a median follow-up of 86 mo, 0.9% of 216 patients with low-risk NMIB, 2.2% of 182 patients with intermediate-risk NMIB, and 9.8% of 193 patients with high-risk NMIB developed UUTTs (LE 3) [51]. Patients with a IS are at a significantly higher risk of developing UUTTs. In an analysis of 138 patients with bladder IS, 24.6% developed a UUTT during mean follow-up of

6 EUROPEAN UROLOGY 62 (2012) Table 3 Incidence of upper urinary tract tumours after treatment of non muscle-invasive bladder tumour Author Year Patients, no. UUTT incidence, % Time to diagnosis of UUTT, mo Follow-up time, mo Yousem et al. [53] Palou et al. [54] NA Herr et al. [56]* >180 Solsona et al. [52] Hurle et al. [51] Millán-Rodríguez et al. [49] UUTT = upper urinary tract tumour; NA = not available. * Patients treated with bacillus almette-guérin only. 94 mo, and 32.2% of those patients had bilateral tumours (LE 3) [52]. The time between the initial TURB and the subsequent diagnosis of a UUTT varies among different series (Table 3) [53,54]. In a study by Palou et al, the increased incidence was shown in the first mo after TURB (63.3% of 30 cases) [55]. In a study by Herr et al. of 86 patients treated with BG and followed for 15 yr, 21% of the patients had UUTTs after a median of 7.3 yr (range: 1 15). The majority of UUTTs were invasive, and seven patients (8%) died of disease. Based on this finding, the authors suggest the need for lifelong surveillance of the upper tract in patients with bladder IS (LE 3) [51,56]. T urography and intravenous urography are standard examinations for the exploration of the upper urinary tract; T urography has replaced intravenous excretory urography in many places but carries a larger radiation exposure (LE 4) [57]. An alternative is MRI urography. A yearly investigation of the upper tract is recommended in patients during follow-up for high-risk tumours, including IS [1]. In patients with intermediate-risk tumours, imaging of the upper tract should be considered every 2 yr, while low-risk patients do not need upper urinary tract follow-up (GR B) onclusions Follow-up after TURB for NMIB is necessary because of the significant risk of recurrence and progression. All follow-up recommendations are based on studies with low LEs. ystoscopy remains the standard method for follow-up. The procedure should be done 3 mo after TURB (or re-turb) in all patients. After that, the frequency of check cystoscopies should be tailored according to the individual risk of recurrence and progression. Low-risk patients can be discharged from cystoscopic follow-up after being free of recurrence for 5 yr; alternative methods of assessment may be considered thereafter. In patients with a history of high-risk NMBI, including IS, urinary cytology should be used as an adjunct to cystoscopy, and lifelong bladder follow-up, as well as yearly upper tract imaging, is needed. Urine markers at present have no evidence-based role in the follow-up of NMBI. A follow-up regimen for intermediate-risk patients is less clearly definable and should lie somewhere in between low- and high-risk regimens, according to the current guidelines (Tables 4 and 5) Follow-up for muscle-invasive bladder cancer after cystectomy Rationale The goal of surveillance after R is twofold: to detect any recurrence and to detect any complications of cystectomy and/or urinary diversion as early as possible. Ideally, the detection of either, with effective treatment, should lead to improved outcomes. Surveillance protocols commonly used are built on observed recurrence patterns from retrospective R series. Prospective trials demonstrating the effectiveness of follow-up after R, and particularly its impact on survival, are lacking Recurrence risk estimation Surveillance protocols after R should reflect the risk of recurrence in the particular patient. Higher-stage and lymph node positive disease are associated with higher recurrence rates and poor survival (LE 3) [58]. These two parameters are therefore used as the standard prognostic factors, but other parameters may be useful as well. In Karakiewicz s nomogram, the standard predictors (pt and pn) were supplemented by other eight additional parameters, and the accuracy of recurrence prediction is increased by approximately 3.2% (LE 3) [59]. Similar results were obtained with the International Bladder ancer Nomogram, which is based on the information from 9000 Ba patients from 12 centres worldwide (LE 3) [60]. The drawbacks of these risk group stratification models are that they are based on retrospective data, that the follow-up regimens used differed, and that the original cystectomy series were not comparable. These nomograms also have not been validated externally and therefore cannot be entirely recommended (GR ) Detection of local recurrence and/or distant metastases The rate of local recurrence after R has been reported to range between 5% and 16.5% within 5 yr after surgery. Most of these recurrences are diagnosed during the first 24 mo [5]. Up to 70% of patients with local recurrence will also have distant metastases. The reported median survival after the diagnosis of a local recurrence is only 4 8 mo despite systemic and local treatment. Approximately 80% of patients die of disease within 1 yr, and only 3.5% experience 5-yr survival [61]. Progression without local recurrence is seen in up to 50% of patients after R. Most of these recurrences occur during

7 296 EUROPEAN UROLOGY 62 (2012) Table 4 Non muscle-invasive bladder cancer follow-up recommendations in the literature Examination Recommendation omment Grade First follow-up cystoscopy Schedule of further cystoscopies Discontinuation of regular cystoscopic follow-up PDD/NBI as a part of follow-up cystoscopy Bladder biopsies under anaesthesia during follow-up ytology FISH Soluble urine markers Imaging of the urinary bladder Upper urinary tract evaluation 3 mo after complete TURB (or re-turb) of the NMIB in every patient in whom re-turb is not indicated Risk-adapted approach Possible in low-risk NMIB after being >5 yr tumour-free Better sensitivities but lower specificities than white light cystoscopy When office cystoscopy is suspect or urinary cytology is positive Should be used in conjunction with follow-up cystoscopy to detect disease that may be missed by a routine cystoscopy (carcinoma in situ, upper tract disease, prostatic urethra involvement) annot replace cystoscopy during follow-up of patients with NMIB No urine marker can safely replace cystoscopy during follow-up of patients with NMIB None of the imaging modalities (USG, T, MRI) have sufficient sensitivity to replace cystoscopy in the follow-up of NMIB patients after TURB Yearly in patients with high-risk tumours, including IS; every 2 yr in patients with intermediate-risk tumours; in low-risk patients, upper urinary tract follow-up is not necessary In high-risk patients, every 3 mo for 2 yr, every 6 mo thereafter until 5 yr, and yearly thereafter; lower-risk categories should have longer interval between cystoscopies onsider alternative methods of assessment in these patients (USG) Not enough data for routine use in follow-up of NMIB patients Not necessary after initial BG with erythematous findings if urine cytology is normal Has low sensitivity in low-grade tumours and interobserver variability Unaffected by BG therapy B The risk of recurrence in the upper urinary tract is lifelong, particularly in patients with IS B B TURB = transurethral resection of the bladder; NMIB = non muscle-invasive bladder cancer; USG = ultrasonography; PDD/NBI = photodynamic diagnosis/ narrow-band imaging; BG = bacillus almette-guérin; FISH = fluorescence in situ hybridization; T = computed tomography; MRI = magnetic resonance imaging; IS = carcinoma in situ. the first 24 mo, although metastases have been observed as late as 10 yr after R. The most likely sites for distant metastases are bones, liver, and lungs. The median survival of patients with progressive disease treated with platinumbased chemotherapy varies between 9 and 26 mo [61]. Despite regular follow-up, a significant number of patients are symptomatic at the time of the diagnosis of recurrence. Of 1388 patients treated at the Mayo linic, 493 (35.5%) experienced recurrence. Symptoms at the time of recurrence were noted in 80% of these patients (LE 3) [62]. Of the 1270 patients followed at Ulm University, 444 developed recurrence, and only one of every three cases was detected in an asymptomatic state, despite the use of advanced imaging including T, MRI, and positron emission tomography (LE 3) [63]. In a separate analysis of the 130 patients with pelvic recurrence after R, it was found that 61.5% were diagnosed because of symptoms and only 38.5% by surveillance T (LE 3) [64]. Table 5 Panel of authors suggested schedule for follow-up in patients with non muscle-invasive bladder cancer Examination Type of NMIB Timing Tools First follow-up visit after TURB/re-TURB All At 3 mo ystoscopy plus cytology in intermediate- and high-risk patients, cystoscopy in low-risk patients Schedule of further visits Low risk If the first follow-up cystoscopy is negative, ystoscopy, after 5-yr US of the bladder then after 9 mo, then yearly up to 5 yr, after 5-yr ultrasound of the bladder yearly Intermediate risk In between high and low risk: 3-mo intervals ytology plus cytology during first year, then 6-mo intervals until 5 yr, then yearly High risk In 3-mo intervals for 2 yr, 6-mo intervals ystoscopy plus cytology up to 5 yr, then yearly Upper urinary Low risk Not necessary Not necessary tract evaluation Intermediate risk In 2 yr after diagnosis, then every 2 yr T or MRI urography or IVU, or just US yearly High risk In 1 yr after diagnosis, then yearly T or MRI urography or IVU NMIB = non muscle-invasive bladder cancer; TURB = transurethral resection of the bladder; US = ultrasonography; T = computed tomography; MRI = magnetic resonance imaging; IVU = intravenous urography.

8 EUROPEAN UROLOGY 62 (2012) It is generally presumed that the detection of tumour recurrence early, in an asymptomatic state with good performance status, should enable early treatment and may have a survival benefit. However, the existing data analysing the value of routine follow-up at predetermined intervals after R concerning a survival benefit are inconclusive. In one series from Bern University, neobladder patients with recurrence after R detected by routine follow-up had a slightly but significantly higher survival probability (LE 3) [65]. Another study from Ulm University failed to demonstrate a significant survival benefit for detecting tumour recurrence early at an asymptomatic stage. The authors suggested that symptom-driven followup may have similar outcomes compared with routine surveillance and may have potentially lower costs (LE 3) [63]. It is important to realise that the studies looking at follow-up after R used different follow-up regimens and different follow-up imaging methods. Therefore, these data are insufficient to make final recommendations. Asymptomatic local recurrence is usually detected by T if it is used as the main imaging modality [66]; MRI urography is a valid alternative. There are no reliable tumour markers for the detection of an upper urinary tract recurrence after cystectomy; the only recommended test is the use of urinary cytology (GR B) [67]. The detection of circulating tumour cells, the use of complementary DNA microarray gene expression profiles, and screening for serum protein patterns using matrix-assisted laser desorption/ionization time-offlight mass spectrometry seem potential perspectives but lack reliable clinical data [68 71] Detection of recurrence in remnant urothelium Urethral recurrence. In male patients, urethral recurrence is detected in approximately 1.5 6% after R, with a mean recurrence-free interval of mo (Table 6) [72 76]. The median overall survival in these patients ranges from 28 to 38 mo, and >50% died because of systemic disease [77 79]. The symptoms of urethral recurrence depend on the type of urinary diversion (microhaematuria and/or changes in urinary stream in patients with orthotopic neobladder and urethral bleeding and/or induration of periurethral tissue in patients with a cutaneous diversion). Reported independent predictors of urethral recurrence were cystectomy for NMIB, prostate involvement, and a history of previously recurrent NMIB [77 79]. The risk of urethral recurrence after urethra-sparing cystectomy in females ranges between 0.83% and 4.3% [80 82]. According to published reports, most cases are detected with symptoms such as haematuria, voiding disturbances, and tumour protrusion from the urethral orifice. The prognosis is dependent on the extent of recurrence [80 82]. The surveillance strategies range from observation alone to monitoring with cytology by urethral washings and urethroscopy. In several studies, there was no reported significant survival difference in patients followed with or without urethral washings [78]. However, a recent large retrospective series reported a highly significant survival advantage in male patients with urethral recurrence diagnosed asymptomatic by follow-up compared with male patients diagnosed by symptoms (LE 3) [83]. Thus, followup of the male urethra should be recommended, and any pertaining symptoms must be investigated. Recurrent IS in the urethra with orthotopic bladder substitution can be treated successfully with intraurethral BG in approximately 80% of patients, while papillary and invasive urethral recurrence should lead to urethrectomy [78]. Fewer data are available on the treatment of urethral recurrences in females. All reported cases were treated with urethrectomy [80 82] Upper urinary tract recurrence. UUTTs occur in 1.8 6% of cases in contemporary series (Table 7) and generally are seen later than urethral recurrence (median time to recurrence: mo). In fact, the upper urinary tract is the most common site of late recurrence (3 yr of diseasefree survival following R) [62,84,85]. The median overall survival is mo, and 60 67% of patients die of metastatic disease [86]. Symptoms of UUTT can be macrohaematuria and/or flank pain, but the most common presentation is the asymptomatic development of unilateral hydronephrosis [86]. Four risk factors for UUTT have been identified: a history of IS, a history of recurrent Ba, R for NMIB, and initial tumour involvement of the distal ureter in the cystectomy specimen. Patients who had none of these risk Table 6 Incidence of urethral recurrence after radical cystectomy Source Year n Urethral recurrence, incidence, % Time to recurrence, mo Follow-up time, mo omment Levinson et al. [72] Tongaonkar et al. [73] NA 19% with orthotopic diversion, 81% with cutaneous diversion lark et al. [74] Stein et al. [75] % with orthotopic diversion, 49% with cutaneous diversion Studer et al. [77] Only orthotopic bladder substitution Hautmann et al. [76] Only orthotopic bladder substitution Huguet et al. [79] % of 219 patients with orthotopic diversion, 5.6% of 510 patients with cutaneous diversion NA = not applicable.

9 298 EUROPEAN UROLOGY 62 (2012) Table 7 Incidence of upper urinary tract tumours after radical cystectomy Source Year n NMIB patients at cystectomy, no. (%) Upper urinary tract recurrence, incidence, % Time to recurrence, mo Follow-up time, mo Huguet-Pérez et al. [84] (17.5) >60 Hautmann et al. [76] NA Meissner et al. [86] (25.7) Sanderson et al. [85] NA Tran et al. [88] (26.4) Volkmer et al. [87] (20.7) Umbreit et al. [62] (30.8) NA NMIB = non muscle-invasive bladder cancer; NA = not applicable. factors had an upper urinary tract recurrence rate of only 0.8% at 15 yr, compared with 13.5% in patients with three to four risk factors (LE 3) [87]. There is a lifelong risk of UUTT after R for MIB. In the Ulm series, the rate of UUTT at 5, 10, and 15 yr was 2.4%, 3.9%, and 4.9%, respectively (level 3) [87]. The 3- and 5-yr cumulative incidence of UUTT in the Memorial Sloan- Kettering ancer entre series was 4% and 7%, respectively. The 3-yr risk of UUTT was approximately 4 6% at any point of time 4 yr after R and did not change over time using a landmark analysis (LE 2b) [88]. Urinary cytology can detect <30% of UUTTs when used for routine postcystectomy surveillance; however, in patients with symptoms, findings are positive in % [87]. The finding of positive cytology may precede a possible imaging diagnosis of UUTT; at the time of the first positive cytology, only 9% (9 of 101) of the patients had UUTT confirmed, but eventually 56% (57 of 101) of these patients developed identifiable UUTT. The median time free from recurrence after positive cytology was 2.1 yr; thus, a positive cytology is highly predictive of upper urinary tract recurrence (LE 3) [89], and cytology is recommended for upper urinary tract follow-up. T urography with MRI urography as an alternative is standard examination of the upper urinary tract after R (Table 8) Follow-up for urinary diversion related complications Apart from the oncologic outcome, there are also metabolic and functional aspects of urinary diversion that warrant follow-up Vitamin B 12 deficiency. Removal of the terminal ileum for the construction of a bladder substitute may predispose patients to vitamin B 12 deficiency. For patients with Table 8 Panel of authors suggested schedule for follow-up in patients with muscle-invasive bladder cancer after cystectomy Time after cystectomy, mo Then yearly pt2 N Blood tests X X X X X X X X X X X X Urine culture X X X X X X X X X X X X ytology X X X X X X X X X X X X Postvoid residual urine * X X X X X X X X X X X X Urethral washing ** X X X X X Vitamin B 12 X X X X Ultrasound X X hest radiograph X X X X X X X Bone scan X T urography X X X X X X X X *** Time after cystectomy, mo Then yearly pt3 or pn Blood tests X X X X X X X X X X X X Urine culture X X X X X X X X X X X X ytology X X X X X X X X X X X X Postvoid residual urine * X X X X X X X X X X X X Urethral washing ** X X X X X X X X X X Vitamin B 12 X X X X Ultrasound X hest radiograph X X X X X X X X X Bone scan X X X T urography X X X X X X X X X X *** T = computed tomographic; NMIB = non muscle-invasive bladder cancer. * Orthotopic bladder. ** Ileal conduit plus retained urethra, cystectomy for NMIB, prostate/bladder-neck involvement, a history of previously recurrent NMIB. *** In newly diagnosed hydronephrosis or if cytology is positive.

10 EUROPEAN UROLOGY 62 (2012) Table 9 Muscle-invasive bladder cancer follow-up recommendations in the literature Diagnosis Recommendation omment Grade Tumour recurrence Local and distal recurrence No recommended follow-up strategy Follow-up at predetermined intervals allows for early treatment and may have survival benefit; should be intensive during first 5 yr after R Urethral recurrence No recommended follow-up strategy All symptomatic patients should be examined with cytology by urethral washings and urethroscopy. Regular follow-up may have survival benefit (if urethral recurrence is diagnosed asymptomatic). Upper urinary tract recurrence No recommended follow-up strategy There is a lifelong risk of UUTT after R for MIB. Positive cytology is highly predictive of upper urinary tract recurrence during follow-up. Functional outcomes Vitamin B 12 deficiency Lifelong parenteral vitamin B 12 Neuropathy due to vitamin B 12 deficiency is irreversible. supplementation in patients with terminal ileal resections in whom 3 yr after operation, vitamin B 12 serum level is <200 pg/ml Metabolic acidosis Urinary diversion related complications Serum evaluation for metabolic acidosis every 3 mo during the first year after R and then every 6 12 mo The risk of diversion-related complications increases with time; lifelong examination for lithiasis, benign stricture, or hydronephrosis is necessary Patients at risk with ileal neobladder, with reduced renal function, postvoid residual urine, and urinary tract infection omplications developed in 45% of patients within the first 5 yr; this percentage increased to 50%, 54%, and 94% in patients surviving 10, 15, and >15 yr, respectively. R = radical cystectomy; UUTT = upper urinary tract tumour; MIB = muscle-invasive bladder cancer. terminal ileal resections >20 cm, B 12 serum levels should be measured. Vitamin B 12 deficiency may lead to megaloblastic anaemia reversible by substitution treatment and irreversible neuropathy. Once vitamin B 12 deficiency has been confirmed, the patient will require its lifelong supplementation (LE 2b) [90]. As the average body deposits of vitamin B 12 are large, vitamin B 12 measurements and/or substitution should be realised from 3 5 yr after R onwards (GR ) Metabolic acidosis. The frequency and severity of metabolic acidosis are usually related to the type and length of intestinal segment used for the construction of a bladder substitute, but symptom severity and the degree of decompensation will also depend on the age of the patient and metabolic ability to compensate. Metabolic acidosis can be expected in 15% of patients with an ileal conduit and in 50% of patients with a continent diversion (LE 3) [91]. The risk of metabolic acidosis is the highest during the early postoperative period, in neobladder patients with postvoid residual urine, with urinary tract infection, and in patients with reduced renal function. The clinical signs of metabolic acidosis can be nausea, lack of appetite, fatigue, and weakness, and ultimately vomiting or accelerated breathing. hronic metabolic acidosis can lead to bone demineralization; thus, attention should be given to bone metabolism in patients with even mild acidosis. Sodium bicarbonate should be given generously (2 6 g/d) from the early postoperative period [91]. As the timing and degree of metabolic acidosis may be variable, no definitive recommendations exist. Serum evaluation for metabolic acidosis should be done regularly during the first 12 mo after R and then probably every 6 12 mo (GR ) Urinary diversion related complications. The risk of diversion-related complications increases with time. The most frequent complications are symptomatic urinary tract infections; urolithiasis; stenosis of the ureterointestinal anastomosis with potential loss of renal function; complications related to the stoma in conduits; and in neobladder patients, urinary retention and day and/or nighttime incontinence. In a series with ileal conduit, complications developed in 45% of patients within the first 5 yr. This percentage increased to 50%, 54%, and 94% in patients surviving 10, 15, and >15 yr, respectively (LE 3) [92] onclusions The early detection of tumour recurrence after R allows for early treatment. As most relapses occur within 5 yr and the median time to local and distant recurrence is mo after R, follow-up should be intensive for the first 5 yr, particularly for the first 2 yr. Patients with extravesical and lymphnod positivediseaseatrhavethehighestriskof recurrence. Regular follow-up of the male urethra by urethral washings and urethroscopy has survival benefit, if urethral recurrence is diagnosed early before symptoms occur. Most upper urinary tract recurrences occur >3 yr after R, at a time when the risk of local and systemic recurrence is decreasing. Lifelong yearly upper urinary tract imaging is advisable in all patients. This study also allows for early detection of urinary diversion complications. Metabolic evaluation should continue throughout life, and vitamin B 12 substitution should commence from 3 5 yr after surgery (Tables 8 and 9). In general, the studies about follow-up after R are low LE and based on retrospective data. Nonetheless, reasonable recommendations can be made until further prospective randomised

11 300 EUROPEAN UROLOGY 62 (2012) studies that test different follow-up schedules have been performed. 4. onclusions Follow-up in Ba is necessary for diagnosing recurrence and progression as well as for evaluating complications after radical treatment. Since randomised studies investigating the most appropriate follow-up schedule are lacking, most recommendations are based on only the retrospective experience. Nonetheless, reasonable recommendations can be made until further prospective randomised studies testing different follow-up schedules have been performed. Author contributions: Viktor Soukup 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: Soukup, Babjuk, Bellmunt, Dalbagni, Giannarini, Hakenberg, Herr, Lechevallier, Ribal. Acquisition of data: Soukup, Babjuk, Bellmunt, Dalbagni, Giannarini, Hakenberg, Herr, Lechevallier, Ribal. Analysis and interpretation of data: Soukup, Babjuk, Bellmunt, Dalbagni, Giannarini, Hakenberg, Herr, Lechevallier, Ribal. Drafting of the manuscript: Soukup, Babjuk, Bellmunt, Dalbagni, Giannarini, Hakenberg, Herr, Lechevallier, Ribal. ritical revision of the manuscript for important intellectual content: Soukup, Babjuk, Bellmunt, Dalbagni, Giannarini, Hakenberg, Herr, Lechevallier, Ribal. Statistical analysis: None. Obtaining funding: None. Administrative, technical, or material support: Soukup. Supervision: Babjuk, Bellmunt, Dalbagni, Giannarini, Hakenberg, Herr, Lechevallier, Ribal. Other (specify): None. Financial disclosures: Viktor Soukup certifies 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] Babjuk M, Oosterlinck W, Sylvester R, et al. EAU guidelines on nonmuscle-invasive urothelial carcinoma of the bladder, the 2011 update. Eur Urol 2011;59: [2] Sylvester RJ, van der Meijden APM, Oosterlinck W, et al. Predicting recurrence and progression in individual patients with stage TaT1 bladder cancer using EORT risk tables: a combined analysis of 2596 patients from seven EORT trials. Eur Urol 2006;49: [3] Fernandez-Gomez J, Madero R, Solsona E, et al. 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