Second transurethral resection against Ta high grade tumor:residual location and predictive factor. A single center, retrospective study

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1 Japanese Journal of Endourology(2018)31: Original Article CJapanese Society of Endourology 2018 Tetsuya Shindo Naotaka Nishiyama Naoya Masumori Second transurethral resection against Ta high grade tumor:residual location and predictive factor. A single center, retrospective study Abstract Purpose:To evaluate the residual tumor rate and location in second transurethral resection after Ta high-grade bladder cancer. Patients and methods:patients with Ta high-grade bladder cancer were evaluated retrospectively. Thirtynine patients had Ta high-grade bladder cancer and received a second TUR at our institution. Results:Ten of the 39(25.6%)patients had residual cancer. Tumor diameter of less than 10 mm was a predictive risk factor for residual cancer at the 2 nd TUR in multivariate analysis(p=0.009). Seven of the 10(70%) patients with residual cancers were detected at the edge of the initial TUR scar, and 2 patients cancers were found at the edge of the 2 nd TUR resection lesion. Conclusion:Residual cancers were mostly located around the initial and 2 nd TUR resection areas. Wide resection should be performed in the 2 nd TUR for a Ta high-grade tumor even if the tumor is small at the initial TUR. Key words:second TUR, high grade Ta, bladder cancer Introduction Transurethral resection of a bladder tumor(turbt) is an essential and critical procedure not only for diagnosing stage and grade but also to cure non-muscle invasive bladder cancer(nmibc). Even with an appropriate surgical procedure, the recurrence rate is relatively high in NMIBC 1). Although most NMIBC is not fatal, it may progress to muscle-invasive bladder cancer(mibc), Tetsuya Shindo Naotaka Nishiyama Naoya Masumori: Department of Urology, Sapporo Medical University School of Medicine, Sapporo, Japan Correspondence and Galley proofs:tetsuya Shindo, M.D. Department of Urology, Sapporo Medical University School of Medicine S 1 W16, Chuo-ku, Sapporo, Japan Tel ext , FAX shindo1013@yahoo.co.jp Received;22 June 2017;accepted in final form 26 September 2017 which can lead to death from cancer 2). Because of the high residual tumor rate and detection of MIBC, a 2 nd TUR is a standard strategy against T1 or high-grade bladder cancer and is reported to reduce the recurrence rate of NMIBC and potentially inhibit progression to MIBC 3-5). To prevent recurrence and progression in NMIBC, a 2 nd TUR is widely recommended 6). In addition to high-grade tumors and pt1 tumors, bladder cancer without a definitive muscle layer in the specimen has a worse outcome and a 2 nd TUR is recommended 6, 7). Although the 2 nd TUR is a standard procedure, reports on it have mostly focused on T1 high-grade bladder cancer. On the other hand, the outcome of the 2 nd TUR for TaHG bladder cancer is rarely reported, especially in Asian countries. Therefore, we investigated the outcomes of the 2 nd TUR for TaHG tumors. Materials and Methods We retrospectively evaluated patients who underwent TURBT between January 2007 and January Among 57 patients with TaHG bladder cancer, 39 patients received a 2 nd TUR at our institution(group 1) and 18 patients did not(group 2). All specimens were evaluated by experienced pathologists in our institution. High-grade bladder cancer was determined according to the 2004 WHO criteria 8). Patients who could not have all visible tumors resected in the initial TUR procedure or having a history of MIBC were excluded. Patients who mainly had adenocarcinoma or squamous cell carcinoma in specimens were also excluded. The definition of recurrence was intravesical recurrence and progression was defined as MIBC or having distant or lymph node metastasis. At the time of the initial and 2 nd TUR procedures, we performed biopsy at the edge of the resection line without cauterization to evaluate the margin status. We also obtained specimens from the bottom of the resection area to evaluate the possibility of cancer in the muscle layer. For the 2 nd TUR, we first marked a circular resection line about 7-8 mm wide around the initial TUR scar(fig. 1). After resection of the marked area, we performed a cold biopsy at the edge of the margin and at the bottom 108

2 Second transurethral resection against Ta high grade tumor:residual location and predictive factor. A single center, retrospective study Statistical analyses were performed using SPSS version This study was approved by the institutional review board in our hospital(no ). Fig. 1 Schematic of resection and tissue sampling around the edge of the resection area for the initial and 2 nd TUR. of the area so that we could evaluate the margin status and existence of MIBC in the detrusor muscle. We separated these specimens into different containers in order to diagnose the cancer location accurately. Random biopsy was performed at the initial TUR. However, if the tumor was smaller than 10 mm and solitary with negative cytology, it was omitted. Random biopsy was not performed at the 2 nd TUR. However, resection or biopsy was done if a suspicious lesion such as one with a reddish appearance was observed. Statistical analysis was performed using the chisquare, student T tests, and Mann-Whitney tests, with the log-rank test used for intergroup comparisons. Logistic regression analysis was performed to evaluate predictive factors for residual tumors at the 2 nd TUR. All values were considered statistically significant at P<0.05. Results Intergroup analysis is shown in Table 1. Only BCG instillation was significantly different between the groups, with group 1 having a higher rate. The follow-up periods ranged from 3-96 months(median 19 months) in group 1 and 3-62 months(median 18.5 months)in group 2. The clinical outcomes after TURBT and results of the 2 nd TUR are shown in Table 2. Seven of the 39 (17.9%)patients had recurrence during the follow-up period in group 1, as did 5 of the 18(27.8%)patients in group 2. No progression or cancer death was observed in either group. Nine of the 10 patients who had residual cancer in the 2 nd TUR had pta bladder cancer. No MIBC was found at the 2 nd TUR. Intravesical recurrencefree survival did not differ between the groups(fig. 2, p=0.465, log-rank test). Tumor diameter of less than 10 mm was a predictive risk factor for residual cancer at the 2 nd TUR in univariate analysis(table 3, p=0.017, Fisher s exact probability test)and multivariate analysis (Table 4, P=0.009, logistic regression analysis). Of the 10 patients with residual cancers, 7 tumors were detected at the edge of the initial TUR scar(fig. 1, area 1)and 2 were at the edge of the 2 nd TUR resection area(fig. 1, area 2). One was in a different area from the initial resection(fig. 1, area 3). Table 1 Characteristics of the patients by group. Group 1 Group2 P value (with 2 nd TUR) (without 2 nd TUR) Age ** (median 66) (median 66) Sex Male 29(74.4%) 16(88.9%) Female 10(25.6%) 2(11.1%) Tumor size 0.479** Less than 10 mm 11(28.2%) 5(27.8%) 10mm or more and less than 20mm 17(43.6%) 10(55.5%) 20mm or more 11(28.2%) 3(16.7%) Multiplicity Solitary 17(43.6%) 10(55.6%) Multiple 2(56.4%) 8(44.4%) Concomitant CIS Yes 5(12.8%) 3(16.7%) No 34(87.2%) 15(83.3%) BCG instillation * Yes 32(82.1%) 6(33.3%) No 7(17.9%) 12(66.7%) Follow up period ** (months) (median 19) (median 18.5) (Fisher s exact probability test, *chi-square test, **Mann-Whitney U test) 109

3 Table 2 Outcome of 2 nd TUR and clinical course by group. Group 1 Group 2 (with 2 nd TUR) (without 2 nd TUR) Residual Tumor 10(25.6%) Not existed in 2 nd TUR Residual Tumor (pt stage) Tis 1(2.6%) Not existed Ta 9(23%) T1 or more 0(0%) Recurrence Yes 7(17.9%) 5(27.8%) No 32(82.1%) 13(72.2%) Progression Yes 0 (0%) 0(0%) No 39(100%) 18(100%) Cancer death Yes 0(0%) 0(0%) No 39(100%) 18(100%) Fig. 2 test). Recurrence-free survival according to group(log-rank Table 3 Univariate analysis of predictive factors for residual cancer in 2 nd TUR. Factors Residual Residual P value tumor(+) tumor(-) N=10 N=29 Tumor size Less than 10 mm 6(60%) 5(17.2 %) 10 mm or more 4(40%) 24(82.8 %) Multiplicity Solitary 2(20%) 16(55.2%) Multiple 8(80%) 13(44.8%) Concomitant CIS Yes 1(10%) 4(13.8%) No 9(90%) 25(86.2%) Morphology Papillary and pedunculated 7(70%) 23(79.3%) Others 3(30%) 6(20.7%) 1 st TUR SMU 9(90%) 26(89.7%) Others 1(10%) 3(10.3%) (Fisher s exact probability test)smu:sapporo Medical University. Table 4 Multivariate analysis of predictive factors for residual cancer in 2 nd TUR. Factors HR(95%CI) P value Tumor size less than10 mm ( ) Multiple tumor ( ) Concomitant CIS(+) ( ) Not papillary and pedunculated appearance ( ) 1 st TUR at SMU ( ) (Logistic regression analysis)smu:sapporo Medical University. 110

4 Second transurethral resection against Ta high grade tumor:residual location and predictive factor. A single center, retrospective study Discussion According to the 2004 WHO/ISUP pathological grading system, high-grade Ta bladder cancer, which was previously diagnosed as Ta grade 3 or partly grade 2, is diagnosed as a TaHG tumor. Lokeshwar et al. reported the impact of the 2004 ISUP/WHO classification on TaHG bladder cancer, which increased between 2007 and ). TaHG bladder cancer is reported to occur in % of all bladder cancers 10, 11). The EAU guideline strongly recommends performing a 2 nd TUR for these high-grade tumors 6). However, these tumors and the outcome of the 2 nd TUR for them are not well understood because they are relatively rare. Thus, to analyze the clinical outcomes of the procedure for TaHG is important. The clinical benefits of a 2 nd TUR are widely accepted and it has become a gold standard strategy, especially for T1 high-grade tumors. Originally it was mostly performed 4 to 6 weeks after the initial TUR and the purpose was to detect MIBC in patients who were diagnosed with T1 bladder cancer at the initial TUR 4, 5). The recurrence rate is reduced in patients who undergo a 2 nd TUR compared to those without it 12). Second TUR might also inhibit progression to MIBC 13). Lazica et al. and Herr et al. reported that % of TaHG bladder cancers were MIBC in the 2 nd TUR 11, 14). The question remains, however, how a TaHG tumor can result in MIBC after appropriate initial TUR with a wide margin and a definite muscle layer in the specimen. It is unlikely that these patients who had MIBC in the 2 nd TUR were treated appropriately at the initial TUR with a definitive muscle layer in the specimen. The residual cancer rates(from 27 to 65%)in the 2 nd TUR for TaHG bladder cancer had a wide range in previous reports 14, 15). The wide ranges of upstaging and the residual cancer rate may be due to the experience of the surgeons. It is known that the quality of TUR differs according to the surgeon s experience. Mariappan et al. reported that the rate of obtaining detrusor muscle in the TUR procedure, which represents the quality of TUR, was better for experienced surgeons 16). Experienced surgeons obtained detrusor muscle from 51 of 73(68.9%)patients, whereas the rate was was 23 of 72(31.1%)patients for less experienced surgeons(p<0.001). Detrusor muscle in the TUR specimen is also reported to be a predictive factor for progression to MIBC, especially in T1G3 bladder cancer 7). It is crucial to compensate for the difference in the quality of the procedure to accurately evaluate the clinical outcome of 2 nd TUR for TaHG tumors. Thus, we performed the initial and 2 nd TUR uniformly as mentioned above. This uniform procedure made it possible not only to evaluate the margin status but also urothelial cancer in the muscle layer. We speculate, therefore, that this is the reason we did not have upstaging to MIBC at the 2 nd TUR. In the present study, the predictive factor for residual cancer at 2 nd TUR was small tumor size of less than 10 mm. Although not statistically significant, with multiple tumors there was a tendency for there to be residual cancer(table 4, p=0.068, logistic regression analysis). Lazica et al. also reported that with a tumor size of less than 30 mm there was a tendency for there to be residual tumors in the 2 nd TUR for TaHG bladder cancer 11) The residual tumors were mostly detected at the 2 nd TUR (7/10, 70%)in area 1(Fig. 1), which was adjacent to the initial TUR area. Furthermore, 2 of the 10 residual tumors were detected at the edge of the 2 nd TUR area (Fig. 1, area 2). Previous studies reported that about 80% of residual tumors were detected in the initial resection site 3, 4), especially at the bottom of the initial scar 17). However, we found that the residual tumors in TaHG bladder cancer were around the initial resection site rather that at the bottom of it. TaHG tumors have been reported to have a higher concomitant CIS rate than low-grade tumors(26.1% vs. 2.5%) 11). Thus TaHG tumors may have a different biological character from Ta low-grade tumors and might have wide tumor spread or daughter tumors that are not visible around the main tumor. TaHG might also have a higher risk of CIS than Ta low-grade tumors. This suggests that a wide margin around the initial tumor should be resected even if the tumor is relatively small. Although it is clear that TaHG tumors have residual cancer in the 2 nd TUR, our data could not clarify the effect of the intravesical BCG instillation therapy and 2 nd TUR on intravesical recurrence. This might have been due to the small sample size and relatively short followup period, which are limitations of our study. As other limitations, our study was retrospective and the BCG instillation rate differed between the groups. Most of the patients in group 2 did not undergo a 2 nd TUR because of the patient s refusal, which might have resulted in selection bias. Conclusion A second TUR after TaHG bladder cancer revealed residual cancer without upstaging in 25.6% of the cases. Because 70% of the residual cancer was located around the initial TUR resection lesion, a wide resection margin is required at the 2 nd TUR for TaHG tumors. Disclosure The authors have nothing to disclose. References 1) Hoglund M(2007)On the origin of syn- and metachronous urothelial carcinomas. Eur Urol 51: ) Kullkarni GS, Hakenberg OW, Gschwend JE, et al.(2010)an updated critical analysis of the treatment strategy for newly diagnosed high-grade T1(previously T1G3)bladder cancer. Eur Urol 57:

5 3) Schwaibold HE, Sivalingam S, May F, et al.(2006) The value of a second transurethral resection for T1 bladder cancer. BJU Int 97: ) Sivalingam S, Probert JL, Schwaibold H(2005) The role of repeat transurethralresection in the management of high-risk superficial transitional cellbladder cancer. BJU Int 96: ) Miladi M, Peyromaure M, Zerbib M, et al.(2003) The value of a second transurethral resection in evaluating patients with bladder tumours. Eur Urol 43: ) Babjuk M, Burger M, Zigeuner R, et al.(2013) EAU guidelines on non-muscle invasive urothelial carcinoma onf the bladder:update Eur Urol: ) Shindo T, Masumori N, Kitamura H, et al.(2014) Clinical significance of definite muscle layer in TUR specimen for evaluating progression rate in T1G3 bladder cancer:multicenter retrospective study by Sapporo Medical University Urologic Consortium (SUOC). World J Urol: ) Montironi R, Lopez-Beltran A(2005)The 2004 WHO classification of bladder tumors:a summary and commentary. Int J Surg Pathol: ) Lokeshwar SD, Ruiz-Cordero R, Hupe MC, et al.(2015)impact of 2004 ISUP/WHO classification of bladder cancer grading. World J Urol: )Sylvester RJ, van der Meijden A, Witjes JA, et al.(2005)high-grade Ta urothelial carcinoma and carcinoma in situ of the bladder. Urology 66(suppl 1): )Lazica DA, Roth S, Brandt AS, et al.(2011)second transurethral resection after Ta high-grade bladder tumor:a 4.5-year period at a single university center. Urol Int: )Divrik RT, Yildrim U, Zorlu F, et al.(2006) The effect of repeat transurethral resection on recurrence and progression rates in patients with T1 tumours of the bladder who received intravesical mitomycin;a prospective, randomized clinical trial. J Urol: )Divrik RT, Sahin AF, Yildrim U, et al.(2010) Impact of routine second transurethral resection of the long-term outcome of patients with newly diagnosed pt1 urothelial carcinoma with respect to recurrence, progression rate, and disease-specific survival:a prospective randomized clinical trial. Eur Urol: )Herr HW(2011)Role of re-resection in non-muscleinvasive bladder cancer. Scientific World-Journal 11: )Zurkirchen MA, Sulser T, Gaspert A, et al.(2004) Second transurethral resection of superficial transitional cell carcinoma of the bladder:a must even for experienced urologists. Urol Int: )Mariappan P, Finney SM, Head E, et al.(2011) Good quality white-light transurethral resection of bladder tumours(gq-wlturbt)with experienced surgeons performing complete resections and obtaining detrusor muscle reduces early recurrence in new non-muscle-invasive bladder cancer:validation across time and place and recommendation for benchmarking. Int BJU 109: )Jakse G, Algaba F, Malmstrom PU, et al.(2004)a second-look TUR in T1 transitional cell carcinoma: why? Eur Urol 45:

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