Background: This study was conducted to determine whether the location of the bladder neck in postoperative cystography predicts recovery of continence after radical prostatectomy. Methods: Between 2008 and 2015, 203 patients who underwent laparoscopic radical prostatectomy (LRP, n = 99) and robot assisted radical prostatectomy (RARP, n = 104) were analyzed. The location of the bladder neck was visualized by postoperative routine cystography, and quantitative evaluation of the bladder neck position was performed according to the bladder neck to pubic symphysis (BNPS) ratio proposed by Olgin et al. (J Endourol, 2014). Recovery of continence was defined as no pad use or one security pad per day. To determine the predictive factors for recovery of continence at 1, 3, 6 and 12 months, several parameters were analyzed using logistic regression analysis, including age (≤68 vs. > 68, BMI (≤23.4 vs. > 23.4 kg/m ), surgical procedure (LRP vs. RARP), prostate volume (≤38 vs. > 38 mL), nerve-sparing technique, vesico-urethral anastomosis leakage, and BNPS ratio (≤0.59 vs. > 0.59). Results: The mean postoperative follow-up was 1131 days (79–2880). At 1, 3, 6 and 12 months after surgery, continence recovery rates were 25, 53, 68 and 81%, respectively. Although older age (> 68) and RARP were significant risk factors for incontinence within 3 months, neither was significant after 6 months. A high BNPS ratio (> 0.59) was the only significant risk factor for the persistence of incontinence at all observation points, up to 12 months. Conclusions: A lower bladder neck position after prostatectomy predicts prolonged incontinence. Keywords: Bladder neck location, Radical prostatectomy, Continence recovery Background factors predicting postoperative continence recovery, in- Rates of detection of localized prostate cancer have in- cluding the patient’s age [1–3], BMI [2, 4], prostate size creased with early detection using serum PSA screening , nerve-sparing technique , vesico-urethral anasto- and this in turn has led to increased numbers of radical mosis leakage , and so on. Various procedures have prostatectomies. Postoperative urinary incontinence may been reported to prevent postoperative incontinence, occur in a proportion of patients who undergo radical however, surgeons have not been able to overcome this prostatectomy and is one of the most serious complica- complication completely . tions impacting the quality of life of patients. Several In some institutions, postoperative cystography is per- clinical characteristics have been reported to be critical formed routinely before removing the Foley catheter to confirm no vesico-urethral anastomosis leakage. Several * Correspondence: email@example.com physicians have reported that the postoperative cysto- Department of Urology, Shiga University of Medical Science, Seta gram findings predict continence after radical Tsukinowa-cho, Otsu, Shiga 520-2192, Japan © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kageyama et al. BMC Urology (2018) 18:52 Page 2 of 7 prostatectomy [8–12]. In their prostatectomy series, Table 1 Patients’ characteristics and operative data Jeong et al. reported that the vesico-urethral anastomosis Mean age (range) 67.7 (48–76) location (VUAL) visualized by routine postoperative Mean BMI (kg/m2), (range) 23.7 (16.6–33.2) cystography correlated with early recovery of postopera- Mean preoperative PSA (ng/mL), (range) 9.21 (2.24–43.20) tive continence . They showed a higher location of Clinical T stage, (%) the bladder neck was correlated with better recovery of T1b 3 (1.5) continence. Olgin et al. also reported a similar finding, T1c 122 (60.1) using their original quantitative evaluation of the bladder neck position in a routine cystography after RARP . T2a 45 (22.1) In this study we investigated whether the location of T2b 15 (7.4) the bladder neck in postoperative cystography in our T2c 18 (8.9) LRP and RARP series predicted recovery of continence D’Amico Risk Criteria, (%) within 12 months of surgery. Low risk 40 (19.7) Intermediate risk 108 (53.2) Methods Two hundred and three patients who underwent LRP (n High risk 55 (27.1) = 99) and RARP (n = 104) for clinically localized prostate Operation procedure, (%) cancer in the Shiga University of Medical Science Hos- Laparoscopic 99 (48.8) pital from 2008 to 2015 were evaluated. All clinical, Robot-assisted 104 (51.2) pathological and radiographical data were collected from Nerve-sparing, (%) medical records. The patients’ demographics are pre- Bilateral 24 (11.8) sented in Table 1. This retrospective observational study was approved by the internal ethical committee of Shiga Unilateral 61 (30.0) University of Medical Science. Non-sparing 118 (58.1) The surgical procedure briefly is as follows: The Mean operative time (min), (range) 257 (137–612) Retzius space was approached extraperitoneally (LRP) or Mean estimated blood loss (g), (range) 378 (10–2431) transperitoneally (RARP) and an antegrade radical pros- Mean prostate volume (mL), (range) 41 (18–92) tatectomy was performed with bilateral pelvic lymph Positive surgical margin, (%) 56 (27.5) node dissection. A nerve-sparing technique was indi- cated individually according to various conditions, in- Vesicourethral anastomosis leakage, (%) 16 (7.9) cluding PSA value, Gleason score, number and location Mean Postoperative followup (days) 1131 (79–2880) of positive cores and the patient’s desire to preserve sex- ual function. Bilateral and unilateral nerve-sparing tech- niques were performed in 10 (12%) and 24 (30%) cases, evaluated cystograms and determined the BNPS ratio. Re- respectively. The vesico-uretharal anastomosis was per- covery of continence was defined as wearing no pad or formed with a Van Velthoven running suture. All pa- using one safety pad per day. tients underwent posterior and anterior reconstructions. Univariate analyses were performed using student Cystography was carried out routinely six days after sur- t-test or the chi-square test. Uni- and multivariate logis- gery. Images were obtained in the supine position without tic regression analyses were also performed. When abdominal straining and the bladder was filled with ~ p-values were less than 0.25 in univariate logistic regres- 100 mL of diluted contrast medium. A Foley catheter was sion analysis, the variable was included in the next advanced a few centimeters into the bladder in order to multivariate logistic regression analysis. These statistical visualize the bladder neck clearly. When vesico-urethral analyses were carried out using IBM SPSS Statistics ver- anastomosis leakage was observed, catheter removal was sion 22 software (IBM Japan, Tokyo, Japan). A P-value delayed and a repeat cystography was performed every less than 0.05 is considered statistically significant. week until the leakage resolved. To evaluate the position of the bladder neck quantitatively, we calculated the blad- Results der neck to pubic symphysis (BNPS) ratio, as proposed by The mean postoperative follow-up period was 1131 days Olgin et al. . The BNPS ratio was calculated by meas- (79–2880). Vesico-urethral anastomosis leakage was ob- uring the distance from the superior edge of the pubic served in 16 cases (8%) and catheter removal was de- symphysis to the bladder neck and dividing this by the layed in these patients. Thereafter, repeat cystography total pubic symphysis length in the cystogram. A repre- was performed every week until the leakage resolved. sentative cystogram is shown in Fig. 1. A single physician The mean catheter replacement period was 19.7 days (SKa), who was blinded to the clinical data of the patients, (11–36) in the patients with anastomosis leakage. A Kageyama et al. BMC Urology (2018) 18:52 Page 3 of 7 criteria, nerve-sparing procedure, operative time, esti- mated blood loss, prostate volume, positive surgical mar- gin, anastomosis leakage and BNPS ratio were compared between continent and incontinent patients (Table 2 and Additional file 1: Tables S1-S4). At 1 month after sur- gery, the patient’s age, operation procedure and BNPS ratio differed significantly between the continent and in- continent groups. At 3 and 6 months, the patient’s age and BNPS ratio were significantly different. However, at 12 months, only the BNPS ratio was differed signifi- cantly between the groups. The difference of mean BNPS ratio between the continent and incontinent groups was significant at all evaluation points (Fig. 3). Next, in order to elucidate the risk factors for delayed recovery of continence, we evaluated our patients’ data by logistic regression analysis. According to the risk fac- tors reported previously in the literature, we chose sev- eral variables for analysis, including the patient’s age, BMI, nerve-sparing technique, prostate volume, vesico-urethral anastomosis leakage and BNPS ratio. In addition, we included the surgical procedure, because this showed a significant difference at one month in our cohort. Continuous variables, including age, BMI, pros- Fig. 1 Representative cystogram after surgery tate volume and BNPS ratio, were divided into two cat- egories according to the median values. The median cumulative continence recovery curve of all patients is values of age, BMI, prostate volume and BNPS ratio presented in Fig. 2. The continence status at 1, 3, 6 and were 68y, 23.4 kg/m , 38 mL and 0.59, respectively. In 12 months after surgery was evaluated in an interview order to determine whether other clinical factors were by the physician during regular follow-up visits and the confounding the BNPS ratio, we compared these factors numbers of evaluable patients were 203 (100%), 202 between the high (> 0.59) and low (≤0.59) BNPS ratio (99%), 190 (93%) and 171 (84%), respectively. Contin- ence recovery rates at 1, 3, 6 and 12 months were 25, 53, 68 and 81%, respectively. At each evaluation point, sev- Table 2 Results of statistical analysis of perioperative eral clinical parameters, including the patient’s age, sur- characteristics between continent and incontinent patients at 1, gical procedure, BMI, initial PSA value, D’Amico risk 3, 6 and 12 months Follow-up 1 m 3 m 6 m 12 m Continent (n) 51 107 130 139 Incontinent (n) 152 95 60 32 P-Value Age 0.0020 0.0056 0.0031 0.0512 Procedure 0.0010 0.6601 0.9215 0.3073 BMI 0.5920 0.7470 0.6147 0.8844 PSA 0.3154 0.8596 0.2856 0.7107 D’Amico risk criteria 0.1437 0.4865 0.2614 0.0919 Nerve-sparing 0.2318 0.4737 0.4744 0.3259 Operative time 0.8303 0.7510 0.4918 0.5753 Estimated Blood loss 0.3971 0.2866 0.2039 0.4344 Prostate volume 0.4027 0.5929 0.3245 0.3158 Positive resection margin 0.9801 0.8345 0.3967 0.8450 Anastomosis leakage 0.9906 0.4413 0.1902 0.1285 Fig. 2 Cumulative continence recovery curve of all patients (n = 203) BNPS ratio < 0.0001 0.0006 < 0.0001 0.0003 Kageyama et al. BMC Urology (2018) 18:52 Page 4 of 7 or postoperative factors were also analyzed as predic- tors of post-prostatectomy incontinence and were as follows: nerve-sparing techniques, posterior/anterior reconstruction, bladder neck preservation, periurethral suspension, pelvic floor muscle exercise, incontinence volume at a very early phase after catheter with- drawal, and so on . Postoperative cystography findings also were reported as a predictive factor for continence recovery by a few groups [9–12]. Jeong et al. reported a correlation be- tween VUAL and early continence recovery in a large cohort . They categorized their 678 cases into three groups, based on the vesico-urethral anastomosis loca- tion (VUAL), as determined by postoperative routine cystography: group I - above the upper margin of the Fig. 3 Mean BNPS ratio of the continent and incontinent groups at symphysis pubis, group II – between the upper margin 1, 3, 6 and 12 months after surgery and the middle of the symphysis pubis, and group III – below the middle of the symphysis pubis. Group I groups (Additional file 1: Table S5). The BNPS ratio did showed the best recovery rate, while group III had the not correlate with any other factors. worst continence convalescence. They concluded that a At one month, the univariate logistic regression ana- higher VUAL leads to a higher rate of early continence lysis showed that the older age, RARP and higher BNPS recovery. In their study, they mentioned that the critical ratio correlated with persistent incontinence (Table 3). point of VUAL was the middle of the symphysis pubis. Similarly, a multivariate logistic regression analysis Olgin and colleagues also reported that the higher blad- showed that older age (OR 2.171, 95% CI 1.011–4.663), der neck position correlated with good continence re- RARP (OR 3.131, 95% CI 1.528–6.417) and higher BNPS covery after RARP . They devised a new quantitation ratio (OR 2.867, 95% CI 1.49–5.831) were significant risk parameter, the BNPS ratio, which was calculated on the factors. At three months, the univariate logistic regres- basis of a postoperative cystogram. The BNPS ratios de- sion analysis showed that the older age and higher BNPS rived from the postoperative cystograms of 215 patients ratio correlated significantly with prolonged recovery of who underwent RARP were evaluated and compared continence. Multivariate logistic regression analysis with their continence status. At three months after sur- showed that older age (OR 2.009, 95% CI 1.127–3.581) gery, continent patients had a mean BNPS ratio of 0.39, and higher BNPS ratio (OR 2.245, 95% CI 1.265–3.983) while incontinent patients had a mean BNPS ratio of were significant independent variables. However, at 6 0.49 (p = 0.01). At 12 months, the mean BNPS ratio was and 12 months, only the BNPS ratio was a significant 0.40 for continent patients, whereas incontinent patients predictor in uni- and multivariate logistic regression had a mean BNPS ratio of 0.60 (p = 0.001). The authors analyses. Therefore, the BNPS ratio was the only con- concluded that the BNPS ratio on cystogram correlates stant predictor, not only in short-term but also with continence rates and the lower position of the blad- long-term continence recovery within a year of der neck may predict a risk for prolonged incontinence. prostatectomy. These two studies and the data presented here confirm that the correct suspension of the bladder neck predicts Discussion good recovery of continence and the critical position is Urinary incontinence is a frequent negative outcome of around the middle of the symphysis pubis on a postop- radical prostatectomy and postoperative incontinence erative cystogram. rates of 8~ 20% have been reported in large series [13, What contributes to achieving a higher bladder neck 14]. For patients, recovery of urinary continence is one position after prostatectomy? Extensive studies of pelvic of the most important concerns with respect to quality anatomy have been carried out and much effort has been of life . Several predictive preoperative characteristics devoted to improving surgical techniques. A common have been reported to correlate with recovery of contin- concept pervading these procedures is the conservation ence [1, 2, 7]. In particular, older age, obesity and large of the original anatomical structure. The restoration of prostate volume have been reported as the worst predic- the posterior rhabdosphincter, reported by Rocco et al., tors of continence convalescence. The preoperative ur- was a landmark in the progress of surgical technique ethral length, measured by magnetic resonance imaging, [18, 19]. The authors emphasized that reconstruction of was suggested to be a prognostic factor [16, 17]. Intra- the posterior musclofascial plate and suspension of the Kageyama et al. BMC Urology (2018) 18:52 Page 5 of 7 Table 3 Uni- and multivariate logistic regression analysis of the parameters for incontinence status at 1, 3, 6 and 12 months Follow-up 1 m 3 m 6 m 12 m 1 m 3 m 6 m 12 m Univariate logistic Multivariate regression logistic regression Parameters OR (95% CI) OR (95% CI) P-value P-value Age 2.442 2.102 1.826 1.527 2.171 2.009 1.690 – (< 68 vs. > 68) (1.222–4.881) (1.193– (0.983– (0.706– (1.011–4.663) (1.127– (0.898–3.180) 3.704) 3.392) 3.305) 3.581) P = 0.011 P = 0.010 P = 0.057 P = 0.282 P = 0.047 P = 0.018 P = 0.104 Procedure 3.008 1.132 1.031 1.492 3.131 –– – (LRP vs. RARP) (1.534–5.898) (0.651– (0.559– (0.690– (1.528–6.417) 1.968) 1.901) 3.227) P = 0.001 P = 0.660 P = 0.921 P = 0.309 P = 0.002 BMI 0.843 1.041 0.798 0.483 –– – 0.449 (< 23.4 vs. > 23.4 (0.447–1.592) (0.599– (0.432– (0.219– (0.198–1.017) kg/m2) 1.808) 1.473) 1.064) P = 0.599 P = 0.888 P = 0.470 P = 0.071 P = 0.055 Nerve-sparing 1.474 1.228 1.256 1.493 1.323 –– – (Yes vs. No) (0.779–2.791) (0.700– (0.672– (0.669– (0.634–2.763) 2.154) 2.347) 3.332) P = 0.233 P = 0.474 P = 0.475 P = 0.328 P = 0.456 Prostate volume 1.040 0.921 1.143 0.895 –– – – (< 38 vs. > (0.551–1.961) (0.530– (0.619– (0.415– 38 mL) 1.601) 2.109) 1.933) P = 0.904 P = 0.772 P = 0.669 P = 0.778 Anastomosis 1.007 1.495 2.014 2.389 –– 1.817(0.609– 2.747(0.820– leakage 5.426) 9.198) (No vs. Yes) (0.310–3.274) (0.534– (0.695– (0.756– 4.183) 5.839) 7.551) P = 0.991 P = 0.444 P = 0.197 P = 0.138 P = 0.285 P = 0.101 BNPS ratio 3.127 2.333 2.060 2.371 2.867 2.245 1.989 2.338 (< 0.59 vs. > 0.59) (1.581–6.188) (1.326– (1.103– (1.063– (1.409–5.831) (1.265– (1.056–3.745) (1.034–5.288) 4.106) 3.850) 5.290) 3.983) P = 0.001 P = 0.003 P = 0.023 P = 0.035 P = 0.004 P = 0.006 P = 0.033 P = 0.041 urethral sphincteric complex is the key to the early re- total reconstruction enabled a statistically significant early covery of continence. They reported that their procedure return to continence (38, 83, 91, and 97% at 1, 6, 12, and with posterior reconstruction dramatically shortened re- 24 weeks, respectively) compared with no reconstructive covery periods (72, 79 and 86% at 3, 30 and 90 days procedure (13, 35, 50, and 62%) or with only anterior re- compared with 14, 30 and 46%, respectively, without construction (27, 59, 77, and 86%). They also presented posterior reconstruction) . Another pivotal modifica- typical cystograms of these three groups and the bladders tion is the anterior reconstruction. Various procedures of the total reconstruction group showed the highest were reported by a number of surgeons, including periure- vesico-urethral junctions . Therefore, the suspension thral suspension stitch , preservation of puboprostatic and stabilization of the bladder neck by anatomical recon- collar  and puboprostatic ligament preservation . struction was believed to contribute to an early return of Later, some authors reported on the importance of the continence. All of our cases were performed with both total reconstruction procedure, which includes both anter- posterior and anterior reconstructions. Consequently, it ior and posterior reconstructions. Tewari et al. presented was not possible to differentiate these cases from patients the results of a prospective study to compare continence without the use of these techniques. A lower bladder neck recovery rates of no reconstruction, anterior reconstruc- position after surgery might reflect unsuccessful anatom- tion only and total reconstruction . They reported that ical preservation. Kageyama et al. BMC Urology (2018) 18:52 Page 6 of 7 After prostatectomy, most patients achieve final con- Additional file tinence status within 1 year; therefore, we choose the Additional file 1: Table S1. Perioperative characteristics of the postoperative observation points of 1, 3, 6 and 12 months continent and incontinent patients at 1 month. Table S2. Perioperative for our cases. Interestingly, the mean BNPS ratios of characteristics of the continent and incontinent patients at 3 months. both the continent and incontinent groups increased Table S3. Perioperative characteristics of the continent and incontinent patients at 6 months. Table S4. Perioperative characteristics of the gradually over the postoperative period (Fig. 3). Olgin continent and incontinent patients at 12 months. Table S5.Comparison et al. evaluated their patients at 3 and 12 months and re- of perioperative clinical factors between the low- and high-BNPS ratio ported that the mean BNPS ratios of the incontinence groups. (PPTX 51 kb) group were 0.49 and 0.60, respectively. Similar to our re- sult, the BNPS ratio at 12 months was higher than at Abbreviations LRP: Laparoscopic radical nephrectomy; PSA: Prostate specific antigen; 3 months. Taking their and our findings into account, RARP: Robot assisted radical prostatectomy patients with a BNPS ratio of 0.6 or more might consti- tute the poorest group in terms of postoperative incon- Acknowledgements tinence. Naturally, the postoperative bladder neck No financial support was received for this study. position cannot constitute a predictive factor before Availability of data and materials prostatectomy, therefore, the BNPS ratio is not valuable The datasets generated during the current study are not publicly available as a preoperative predictor of incontinence. However, due to ethical restrictions but are available from the corresponding author on reasonable request. the BNPS ratio can be useful as a prognostic factor which may be obtained easily by a routine postoperative Authors’ contributions cystogram and may be useful, for example, to identify SKa has made substantial contributions to the conception and design, acquisition of data and data analysis. He has drafted the manuscript and patients who require strict instructions for postoperative approved the submitted version. TY, NM, SKu, KT, TT, EH, KJ and NM have recovery of continence, such as pelvic floor muscle exer- made contribution to the acquisition of data. AK has made substantial cise. For surgeons, the BNPS ratio might be used as a contributions to study design and revision of the manuscrip. All authors have read and approved the final manuscript. surrogate predictor for the degree of achievement of preservation of anatomical support of the bladder neck/ Ethics approval and consent to participate sphincter complex. Further research on this point is This study was approved by the ethics committee of the Shiga University of needed. Medical Science (27–99). Written informed consent is not necessarily required in this observational non-invasive retrospective study according to Our study has some limitations. First, our data were the local guideline (the Ethical Guidelines for Medical and Health Research obtained from the experience at a single institution and Involving Human Subjects by the Ministry of Health, Labour and Welfare of the number of patient is relatively small. Second, we Japan). evaluated the position of the bladder neck in a restricted Competing interests condition, in that cystography was performed in the su- The authors declare that they have no competing interests. pine position without straining or standing. With in- creased abdominal pressure, the bladder neck Publisher’sNote presumably will present in a lower position. Third, we Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. did not evaluate various other parameters which may correlate with incontinence. Pre- and/or post-operative Received: 11 January 2017 Accepted: 18 May 2018 membranous urethral length, preoperative LUTS, pre- operative incontinence, and the surgeon’s extent of ex- References perience were not evaluated in our series, because of a 1. Novara G, Ficarra V, D'elia C, Secco S, Cioffi A, Cavalleri S, et al. Evaluating lack of adequate data. 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Published: May 30, 2018