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Orgasm‐Associated Incontinence (Climacturia) after Bladder Neck‐Sparing Radical Prostatectomy: Clinical and Video‐Urodynamic Evaluation
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ORIGINAL RESEARCH—ONCOLOGY Orgasm-Associated Incontinence (Climacturia) after Bladder Neck-Sparing Radical Prostatectomy: Clinical and Video-Urodynamic Evaluation jsm_2829
2150..2156
Francesca Manassero, MD, PhD,* Giuseppe Di Paola, MD,* Davide Paperini, MD,* Andrea Mogorovich, MD,* Donatella Pistolesi, MD,* Francesca Valent, MD,† and Cesare Selli, MD, FACS* *Department of Urology, University of Pisa, Pisa, Italy; †Institutes of Hygiene and Epidemiology, University of Udine, Udine, Italy DOI: 10.1111/j.1743-6109.2012.02829.x
ABSTRACT
Introduction. Orgasm-Associated Incontinence (OAI) or climacturia has been observed in male patients maintaining sexual potency after radical prostatectomy and cystectomy. Aim. We investigated the incidence and video-urodynamic aspects of this event in continent and potent patients after bladder neck-sparing (BNS) radical prostatectomy (RP). Main Outcome Measure. Comparing functional and morphological aspects between climacturic and nonclimacturic patients to identify a possible explanation of this unusual kind of leakage that could seriously impact the sexual life after surgery. Methods. In a pool of 84 men, potent and continent at least 1 year after BNS RP, 24 (28.6%) reported climacturia and 7 agreed to undergo video-urodynamic evaluation (group 1), which was performed also in 5 controls (group 2). Those 12 men were also evaluated with 24-hour pad test, 5-item International Index of Erectile Function and International Prostate Symptom Score questionnaires. Results. Functional urethral length (FUL) was significantly lower in the climacturia group (P = 0.02) and time to continence recovery was significantly longer (P = 0.05). No other significant differences were found between the two groups. The radiological appearance of the vesicourethral junction at voiding cystourethrography was similar. Conclusions. To the best of our knowledge, this is the first functional and morphological evaluation of climacturia after RP. In our experience, this event is indirectly associated with a reduced FUL in the sphincter area, although both patients and controls were continent during daily activities. BNS technique seems to reduce time to continence recovery, although climacturic patients need longer time than control patients. Since in our series no rigidity of the vesicourethral anastomosis was radiographically evident, we believe that differences in FUL could explain OAI. Anatomical difference in membranous urethra length could explain the occurrence of this symptom in patients treated with the same surgical technique. Manassero F, Di Paola G, Paperini D, Mogorovich A, Pistolesi D, Valent F, and Selli C. Orgasm-associated incontinence (climacturia) after bladder neck-sparing radical prostatectomy: Clinical and video-urodynamic evaluation. J Sex Med 2012;9:2150–2156. Key Words. Climacturia, Orgasm-Associated Incontinence, Radical Prostatectomy, Urodynamic, Sexual Dysfunction Following Surgery for Prostate Cancer
J Sex Med 2012;9:2150–2156
© 2012 International Society for Sexual Medicine
Functional Evaluation of Climacturia after Pelvic Surgery Introduction
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ith improving surgical technique, nowadays, radical prostatectomy (RP) is a common urological procedure related to low incidence of postoperative morbidity, but high global number of late complications. Historically, urinary incontinence and erectile dysfunction are wellknown and partially accepted complications following RP with a reported rate of 21% and 39.4–56.9%, respectively [1]. In the last decade the quality of sexual life after RP especially concerning orgasm has been the object of the urologist’s attention [2,3]. Orgasm-Associated Incontinence (OAI) or climacturia (surgical complication grade I) [4] has been observed in male patients maintaining sexual potency after RP and cystectomy with neobladder reconstruction. It is more common than originally thought, and its incidence varies between 15.7% and 93% of cases when it is carefully looked for [5–7]. OAI is often not elicited by the treating physician, unlike urinary incontinence or erectile dysfunction, despite the impact that this problem can have on sexual life. In certain circumstances, small volumes of urine loss can have major impact on patients’ quality of life, leading to a great deal of anxiety and embarrassment or modifying sexual practices. The aim of our study was to evaluate from a functional point of view the bladder and the urethra in men with this recently reported postoperative symptom and to better understand its physiology. If it is inconvenient to perform video-urodynamics study during ejaculation, a possible pathogenesis of OAI could be identified comparing the results of the exam carried out in basal condition between climacturic and non-climacturic patients. Therefore, we investigated the prevalence and videourodynamic aspects of male urinary tracts in men who report climacturia, otherwise continent and potent after bladder neck-sparing (BNS) RP, and to the best of our knowledge, this is the first functional and morphological evaluation of bladders in men with this symptom. Material and Methods
Out of all the men who underwent BNS RP by a single surgeon during the period 2007–2009 and screened with a telephone interview, we identified 84 subjects suitable for participation in this study, since they were continent and potent with or without phosphodiesterase type 5 inhibitors at least
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1 year after BNS RP. The RP were carried out with careful dissection with scissors of the circular BN fibers in all patients, using the technique previously described [8]. Urinary continence, subjectively (telephone question) assessed and objectively (24hour pad test) confirmed, was defined as a leakage ⱕ2 g in 24 hours. Potency was defined as 5-item International Index of Erectile Function (IIEF-5) >22 points (out of 25). Climacturia was arbitrarily defined as at least three episodes of urinary leakage at the moment of climax, in patients otherwise completely continent, 1 year after surgery. Twenty-four patients out of 84 (28.6%) reported climacturia, and seven of them agreed to undergo video-urodynamic evaluation (group 1), which was performed also in five control patients (group 2), e.g., potent and continent men following BNS RP without climacturia. Those 12 men were also evaluated with a 24-hour pad test, IIEF-5 and International Prostate Symptom Score (IPSS) questionnaires. The study had been approved by the local Ethics Committee, and all patients signed the informed consent form. Video-urodynamics investigations were performed according to Good Urodynamic Practices/ International Continence Society using the MMS Solar EUREL unit (Eurel srl, Milan, Italy) [9]. Detailed urodynamic session included one initial uroflow with post-voiding residual (PVR), cystometry in a supine position, Valsalva Leak Point Pressure (VLPP) at 250 mL and maximum filling, urethral pressure profilometry with maximum urethral closure pressure (MUCP) and functional urethral length (FUL). The exam was performed with a 9 Fr double-lumen urethral catheter, filling the bladder with contrast material (mean filling rate of 50 mL/minute). Abdominal pressure was recorded using a 12 Fr intra-rectal balloon catheter. The static urethral pressure profile was estimated as well with the patient in the supine position, after cystometry, with bladder full, using a 9 Fr catheter with a mechanical arm at a rate of 1–2 mm/second. The catheter has a single transducer, and a slow steady perfusion rate of 2–10 mL/ minute is maintained during withdrawal of the catheter (Brown and Wickham technique) [10]. For radiological evaluation a digital system (FCR XG 5000 reader, Fujifilm, Fujifilm Corporation, Tokyo, Japan) was used. Contrast material was Visipaque (Iodixanol, GE Healthcare, Little Chalfont, United Kingdom; iodine concentration 320 mg/dL). Examinations were done by recording the urodynamic trace and, periodically, obtaining fluorosJ Sex Med 2012;9:2150–2156
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Manassero et al.
Table 1 Patient demographics and results of clinical and urodynamic tests, showing that the only two differences between climacturic group and control group are the reduced functional urethral length and the longer time to continence recovery in the first one Variable
Group 1 (7 cases) Mean-median (SD)
Group 2 (5 controls) Mean-median (SD)
P
Age at surgery (years) Gleason score IIEF-5 IPSS Q8 Capacity (mL) PVR (mL) Qmax (mL/second) Qmed (mL/second) VLPP (cm H2O) MUCP (cm H2O) FUL (mm) Time to continence (weeks)
64.1–65 6.4–7 22.3–22 6.3–3 1.1–1 475–500 0–0 21–20 8.7–7 93.3–100 60–58 20.3–20 21.1–26.1
61.8–62 6–6 22.2–22 4.2–4 0.8–1 435–450 0–0 26.2–26 14–14 113–105 98.8–96 35.2–35 0–0
0.48* 0.36* 0.93* 0.87* 0.67* 0.28* 0* 0.13* 0.09* 0.18* 0.15* 0.02* 0.02†
(3.89) (1.13) (1.11) (8.75) (1.06) (61.23) (0) (7.50) (3.72) (27.86) (24.71) (4.03) (16)
(5.31) (2.12) (1.30) (2.28) (0.83) (48.73) (0) (2.38) (3.53) (17.17) (44.13) (4.81) (0)
The statistical significance of differences between the two groups of patients was assessed through Wilcoxon rank sum test. The statistical difference between the two groups in time to continence was assessed through the log-rank test. All the analyses were performed using SAS v9.2 (SAS Institute Inc., Cary, NC, USA). *P value of Wilcoxon rank sum test †P value of log-rank test IIEF-5 = 5-item International Index of Erectile Function; IPSS = International Prostate Symptom Score; Q8 = IPSS question 8; PVR = post-voiding residual; VLPP = Valsalva Leak Point Pressure; MUCP = maximum urethral closure pressure; FUL = functional urethral length; SD = standard deviation
copy acquisitions in the presence of symptoms reported by the patient or alterations in the trace.
Statistical Analysis The distribution of the numerical variables among cases and controls were described by their mean ⫾ standard deviation and median. The statistical significance of differences between the two groups of patients was assessed through Wilcoxon rank sum test. The statistical difference between the two groups in time to continence was assessed through the log-rank test. P values < 0.05 were considered statistically significant. All the analyses were performed using SAS v9.2 (SAS Institute Inc., Cary, NC, USA). Results
The two groups were comparable for age at operation (median 65 vs. 62, mean 64.1 ⫾ 3.9 vs. 61.8 ⫾ 5.3 years), Gleason score (median 7 vs. 6, mean 6.4 ⫾ 1.1 vs. 6.0 ⫾ 2.1), a 24-hour pad test (median 0, mean 0), IIEF-5 scores (median 22, mean 22.3 ⫾ 1.1 vs. 22.2 ⫾ 1.3), IPSS (median 3 vs. 4, mean 6.3 ⫾ 8.7 vs. 4.2 ⫾ 2.3), and quality of life, measured by question 8 of IPSS (median 1, mean 1.1 ⫾ 1.1 vs. 0.8 ⫾ 0.8). In the climacturia group, the phenomenon began few months following the operation, at the sexual activity recovery, in almost all intercourses and persisted 1 year after surgery. Both patients and controls presented good bladder capacity (median J Sex Med 2012;9:2150–2156
500 vs. 450, mean 475 ⫾ 61.2 vs. 435 mL ⫾ 48.7) in absence of detrusor overactivity; maximum urinary flow rate (Qmax) at uroflowmetry was similar (median 20 vs. 26, mean 21.0 ⫾ 7.5 vs. 26.2 mL/second ⫾ 2.4) without PVR, as well as VLPP (median 100 vs. 105, mean 93.3 ⫾ 27.9 vs. 113 cmH2O ⫾ 17.2). The mean urinary flow rate (Qmed) was lower among patients with climacturia (7 vs. 14, mean 8.7 ⫾ 3.7 vs. 14 mL/second ⫾ 3.5, P = 0.09). The MUCP at the level of external sphincter was lower in the climacturia group (median 58 vs. 96, mean 60 ⫾ 24.7 vs. 98.8 cm H2O ⫾ 44.1), although not significant (P = 0.15), while FUL was significantly lower (median 20 vs. 35, mean 20.3 ⫾ 4.0 vs. 35.2 mm ⫾ 4.8; P = 0.02), as well as time to continence recovery, higher in the group 1 (median 26.1 vs. 0, mean 21.1 ⫾ 16.0 vs. 0 weeks ⫾ 0; P = 0.02). The observed data are reported in Table 1. The radiological appearance of the vesicourethral junction at voiding cystourethrography was similar in both groups: bladder neck looks relatively closed at rest and a regular opening of external sphincter without anastomotic strictures or rigidity at voiding phase (Figure 1). Discussion
The term of climacturia was introduced for the first time by Lee et al. in 2006 to describe “urine leakage at the moment of climax,” despite that already in 1996 Koeman et al. had described the symptom [11,12]. As well in 2006 the Cleveland group
Functional Evaluation of Climacturia after Pelvic Surgery
Figure 1 Regular radiological appearance of the vesicourethral junction at voiding cystourethrography in a climacturic patient, without difference with control group.
reported this new phenomenon calling it “ejaculatory urine incontinence,” highlighting that a few drops leakage during sexual intercourse could impair the quality of life. The year later Choi et al. implemented the definition with “orgasm associated incontinence” that with climacturia is the term with which it is presently known [13]. It is more common than originally thought when it is carefully looked for. Its incidence varies between 15.7% and 93% of cases depending on the definition used, how it is recorded (mail questionnaires, telephone interview, during physical evaluation), the type of radical surgery (prostatectomy vs. cystectomy, open or laparoscopic), and the duration of the symptom [5–7]. In a study of prevalence and nature of orgasmic dysfunctions after RP, Barnas et al. reported an incidence of incontinence associated with orgasm at any time after surgery in 93% of men, specifying that the leakage occurred always in 16%, occasionally in 44%, and rarely in 33% [6]. OAI occurs more frequently after RP than after radical cystectomy, and it is not related to the surgical technique (open vs. laparoscopic). More common within the first year after surgery, it is more likely to be reported in men complaining orgasmic pelvic pain and penile shortening [13,14]. Choi et al. failed to find an association
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with the extent of nerve-sparing, surgical margins, preoperative and postoperative sexual function, or daytime continence [13]. Although the pathophysiology of OAI has not been specifically studied and it is poorly understood, different explanations have been postulated. Orgasm combines pleasure and physiological changes at the moment of ejaculation. Immediately before orgasm, the internal sphincter with the bladder neck and the external sphincter are closed in unison, generating a high-pressure zone within the prostatic urethra. The ejaculation is the forcible expulsion of seminal contents from the urethral meatus due to the rhythmic contraction of pelvic-perineal musculature: the bladder neck is closed to prevent semen backflow into the bladder, the external sphincter opens suddenly and the high intraprostatic pressure combined with periurethral musculature contraction leads to antegrade sperm propulsion. As the accessory sex glands are removed at RP, these patients are unable to ejaculate, and thus they experience “dry orgasms.” In patients unable to effectively appose the bladder neck, retrograde ejaculation is common. Abouassaly et al. considered that it is probably also the case in patients who undergo RP, where urine can escape from the bladder and be propelled antegrade during ejaculation. This could be either a neurologic phenomenon or an anatomic one [15]. Intrinsic sphincter deficiency has been considered the primary cause of post-RP incontinence. It is attributable to malfunction of the distal urethral sphincter secondary to direct injury to the sphincter, its supporting structures or its neural innervation. However, daytime continence is not associated with OAI, suggesting a different mechanism. There is has a solid scientific reasoning behind this theory, since daily continence depends on external sphincter function, while OAI prevention depends on bladder neck function [13]. If the external urethral sphincter remains the dominant source of continence following RP, at the moment of climax with relaxation of the external urethral sphincter it could be reasonable that urine leakage would occur. Koeman et al. hypothesized that OAI was related to internal sphincter ablation during RP combined with relaxation of the external sphincter at orgasm [12]. What remains unclear with this hypothesis is why not all men after RP and some men after transurethral prostatic resection have climacturia: to our knowledge this has not been described. Lee et al.’s hypothesis is that bladder neck stricture or a J Sex Med 2012;9:2150–2156
2154 smaller caliber urethra would be less likely to leak urine, although their data do not support that bladder neck status and urethral caliber may have a role in determining climacturia [11]. Because orgasmic pain and loss of penile length have been associated with OAI, it is possible that the three dysfunctions have related mechanisms. Barnas et al. suggested that orgasmic pain following RP might be due to bladder neck spasm, similar to what is believed to occur in men with chronic pelvic pain disorder [6]. The assumption is that after RP physiological bladder neck closure at orgasm translates into spasm of the vesicourethral anastomosis, or pelvic floor musculature dystonia. The concept of bladder neck spasm is further enhanced by the success of the uroselective alphablocker tamsulosin for alleviating dysorgasmia [6,13]. Anorgasmia and decreased intensity of orgasm are most probably psychological events, presumably related to diagnosis of prostate cancer and major radical pelvic surgery [6,13]. Mulhall et al. postulated that cavernous nerve injury and the subsequent sympathetic hyperinnervation during autonomic nerve repair for competitive sprouting could be related to loss of penile length in the early stages after surgery. Assuming that the cavernous smooth muscle is highly contractile in response to adrenergic tone, sympathetic overdrive after cavernous nerve injury would result in a hypertonic condition and penile shortening. If the mechanisms underlying dysorgasmia and penile length loss are indeed sympathetically mediated, it is possible that OAI occurs by a similar process [14,16]. Another hypothesis is that a surgical technique that permits better preservation of the urethral sphincter and neurovascular bundles highly decreases the risk of having climacturia after RP [17,18]. Various mechanisms have been suggested, but none has been adequately tested. The present study was undertaken to better elucidate the pathophysiology of this phenomenon. Climacturia is infrequently spontaneously referred to by the patient who experienced it, but it should be investigated by the physician, even if it is very difficult to objectify. We selected patients completely continent in the daytime and potent to increase the reliability of their answers, and to identify the symptom “climacturia” alone. The incidence and prevalence of this condition are highly related to the definition used: we found a prevalence of 28.6% considering only continent and potent patient following RP. This percentage J Sex Med 2012;9:2150–2156
Manassero et al. could be lower considering all patients after radical surgery, but in our opinion only continent patients at the moment of the orgasm can experience this symptom, while the others easily do not recognize it or confuse it with other urine leakage. Mitchell et al. recently reported that the impact of RP on sexual quality of life is not driven exclusively by the return of erectile function, with a 12.1% of a major problem due to incontinence during sexual activity in sexually active men at 24 months [19]. The aim of our study was a morphological and functional evaluation of urinary tracts in men with this phenomenon more than its impact on quality of life. Moreover, there is no orgasm-specific questionnaire; there are numerous sexual function questionnaires, some too burdensome and complex for these type of patients, others designed for assessing erectile function before and after pharmacotherapy, more than assessing orgasmic function (IIEF-5). No differences in IPSS, IPSS question 8, and IIEF-5 emerged between cases and controls. Although both patients and controls were continent during daily activities, comparing the two groups, interestingly, we found statistically significant difference in FUL and in time to continence. Climacturic patients need also longer time to continence recovery compared with control patients, and they present a reduced FUL. Although the association was not statistically significant, climacturic patients presented a trend to have lower MUCP. Nevertheless, we know that anatomical difference in membranous urethra length could explain the occurrence of this symptom in patients treated with the same surgical technique. The part of membranous urethra and intact striated urethral sphincter that is left intact for anastomosis of bladder to urethra after RP may be important for reaching postoperative continence. Myers et al. showed that the external striated urethral sphincter, visually evident with magnetic resonance imaging (MRI), surrounds the urethral segment located between the prostate and the bulb and therefore they proposed the term “sphincteric urethra.” This unique muscular segment, known as membranous urethra, is mostly important for male urinary continence, and should be preserved at RP [20]. From the morphological point of view, neither a rigidity of the vesicourethral anastomosis nor other morphological appearances were radiographically evident in both groups that we studied, although this is a subjective evaluation. Cystoure-
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Functional Evaluation of Climacturia after Pelvic Surgery thrography is a dynamic examination, where the radiologist can appreciate eventual incomplete neck apposition, urethral strictures or anastomotic rigidity, but anatomical modifications of lower urinary tract after radical prostatic surgery do not allow univocal measurement. The trend toward lower MUCP, with the reduced FUL and the increased time to continence, seems to demonstrate that residual function of external sphincter may have a key role in understanding the physiology of this symptom: in climacturic patients the residual sphincter after RP, due either to anatomical differences of sphincteric/ membranous urethra or to surgeon ability to preserve urethral length, is enough for daytime continence, but not for continence at the moment of climax. We are aware of the limitations of the present study. The reduced number of cases and controls is related to the difficulties to convince otherwise healthy individuals to undergo invasive and embarrassing examination, which requires two catheters insertion and contrast bladder infusion. Moreover, the subjective reporting of this symptom by patients motivates our choice to perform the video-urodynamic exam in basal condition instead of during orgasm, not an easily documented and reproducible anatomical and psychological event. The proposal to perform the exam after intracavernous prostaglandin injection, to reproduce a similar situation, in our opinion is not valid because the mechanisms of erection are completely different from those of ejaculation.
The occurrence of this symptom in patients treated with the same surgical technique could be explained by anatomical difference in membranous urethra length, which direct measurement by MRI would represent a further point of interest. Corresponding Author: Francesca Manassero MD, PhD, Department of Urology, University of Pisa, via Paradisa 2, 56124 Pisa, Italy. Tel: +39-050-997745; Fax: +39-050-997745; E-mail: francy_manassero@ hotmail.com Conflict of Interest: None.
Statement of Authorship
Category 1 (a) Conception and Design Francesca Manassero; Davide Paperini; Cesare Selli (b) Acquisition of Data Francesca Manassero; Giuseppe Di Paola; Donatella Pistolesi (c) Analysis and Interpretation of Data Francesca Manassero; Andrea Mogorovich; Francesca Valent
Category 2 (a) Drafting the Article Francesca Manassero; Giuseppe Di Paola; Andrea Mogorovich; Francesca Valent (b) Revising It for Intellectual Content Francesca Manassero; Davide Paperini; Donatella Pistolesi; Cesare Selli
Category 3 Conclusions
Despite the limitation of a restricted number of patients, due to test invasiveness limiting recruitment, to the best of our knowledge, this is the first functional and morphological evaluation of male urinary tract in men reporting climacturia after RP and although these results can be regarded as preliminary, they remain innovative and should contribute to the better understanding of climacturia etiology. In our experience, this event is indirectly associated with a reduced FUL in the sphincter area, although both patients and controls were continent during daily activities. Indeed climacturic patients need longer time than control patients to continence recovery. Since in our series no rigidity of the vesicourethral anastomosis was radiographically evident, we believe that differences in FUL could be the cause of OAI.
(a) Final Approval of the Completed Article Francesca Manassero; Giuseppe Di Paola; Davide Paperini; Andrea Mogorovich; Donatella Pistolesi; Francesca Valent; Cesare Selli
References 1 Coelho RF, Rocco B, Patel MB, Orvieto MA, Chauhan S, Ficarra V, Melegari S, Palmer KJ, Patel VR. Retropubic, laparoscopic and robot-assisted radical prostatectomy: A critical review of outcomes reported by high-volume centers. J Endourol 2010;24:2003–15. 2 Nelson CJ, Deveci S, Stasi J, Scardino PT, Mulhall JP. Sexual bother following radical prostatectomy. J Sex Med 2010;7:129–35. 3 Dubbelman Y, Wildhagen M, Schroder F, Bangma C, Dohle G. Orgasmic dysfunction after open radical prostatectomy: Clinical correlates and prognostic factors. J Sex Med 2010;7:1216–23. 4 Dindo D, Demartines N, Clavien PA. Classification of surgical complications: A new proposal with evaluation in a cohort of 6,336 patients and results of a survey. Ann Surg 2004;240:205– 13.
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2156 5 Martinez-Salamanca GJI, Jara Rascon J, Moncada Iribarren I, Garcia Burgos J, Hernandez Fernandez C. Orgasm and its impact on quality of life after radical prostatectomy. Actas Urol Esp 2004;28:756–60. 6 Barnas JL, Pierpaoli S, Ladd P, Valenzuela R, Aviv N, Parker M, Waters WB, Flanigan RC, Mulhall JP. The prevalence and nature of orgasmic dysfunction after radical prostatectomy. BJU Int 2004;94:603–5. 7 Nilsson AE, Carlsson S, Johansson E, Jonsson MN, Adding C, Nyberg T, Steineck G, Wiklund NP. Orgasm-associated urinary incontinence and sexual life after radical prostatectomy. J Sex Med 2011;8:2632–9. 8 Selli C, De Antoni P, Moro U, Macchiarella A, Giannarini G, Crisci A. Role of bladder neck preservation in urinary continence following retropubic radical prostatectomy. Scand J Urol Nephrol 2004;38:32–7. 9 Schafer W, Abrams P, Liao L, Mattiasson A, Pesce F, Spangberg A, Sterling AM, Zinner NR, van Kerrenbroeck P, International Continence Society. Good urodynamic practices: Uroflowmetry, filling cystometry, and pressure-flow studies. Neurourol Urodyn 2002;21:261–74. 10 Brown M, Wickham JE. The urethral profile pressure. Br J Urol 1969;41:211–7. 11 Lee J, Hersey K, Lee CT, Fleshner N. Climacturia following radical prostatectomy: Prevalence and risk factors. J Urol 2006;176:2562–5. 12 Koeman M, van Driel MF, Schultz WC, Mensink HJ. Orgasm after radical prostatectomy. Br J Urol 1996;77:861–4.
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Manassero et al. 13 Choi JM, Nelson CJ, Stasi J, Mulhall JP. Orgasm associated incontinence (climacturia) following radical pelvic surgery: Rates of occurrence and predictors. J Urol 2007;177:2223– 6. 14 Mulhall JP. Penile length changes after radical prostatectomy. BJU Int 2005;96:472–4. 15 Abouassaly R, Lane BR, Lakin MM, Klein EA, Gill IS. Ejaculatory urine incontinence after radical prostatectomy. Urology 2006;68:1248–52. 16 Mulhall JP, Slovick R, Hotaling J, Aviv N, Valenzuela R, Water WB, Flanigan RC. Erectile dysfunction after radical prostatectomy: Hemodynamic profiles and their correlation with the recovery of erectile function. J Urol 2002;167:1371– 5. 17 Abdollah F, Salonia A, Briganti A, Deho F, Gallina A, Karakiewicz PI, Guazzoni G, Patard J-J, Rigatti P, Montorsi F. Is climacturia following radical prostatectomy associated with surgical technique? J Urol 2008;179:515. 18 Abdollah F, Briganti A, Salonia A, Cestari A, Guazzoni G, Rigatti P, Montorsi F. Re: Orgasm associated incontinence (climacturia) following radical pelvic surgery: Rates of occurrence and predictors. J Urol 2008;180:1187–8. 19 Mitchell SA, Jain RK, Laze J, Lepor H. Post-prostatectomy incontinence during sexual activity: A single center prevalence study. J Urol 2011;186:982–5. 20 Myers RP, Cahill DR, Devine RM, King BF. Anatomy of radical prostatectomy as defined by magnetic resonance imaging. J Urol 1998;159:2148–58.
ORIGINAL RESEARCH—ONCOLOGY Orgasm-Associated Incontinence (Climacturia) after Bladder Neck-Sparing Radical Prostatectomy: Clinical and Video-Urodynamic Evaluation jsm_2829
2150..2156
Francesca Manassero, MD, PhD,* Giuseppe Di Paola, MD,* Davide Paperini, MD,* Andrea Mogorovich, MD,* Donatella Pistolesi, MD,* Francesca Valent, MD,† and Cesare Selli, MD, FACS* *Department of Urology, University of Pisa, Pisa, Italy; †Institutes of Hygiene and Epidemiology, University of Udine, Udine, Italy DOI: 10.1111/j.1743-6109.2012.02829.x
ABSTRACT
Introduction. Orgasm-Associated Incontinence (OAI) or climacturia has been observed in male patients maintaining sexual potency after radical prostatectomy and cystectomy. Aim. We investigated the incidence and video-urodynamic aspects of this event in continent and potent patients after bladder neck-sparing (BNS) radical prostatectomy (RP). Main Outcome Measure. Comparing functional and morphological aspects between climacturic and nonclimacturic patients to identify a possible explanation of this unusual kind of leakage that could seriously impact the sexual life after surgery. Methods. In a pool of 84 men, potent and continent at least 1 year after BNS RP, 24 (28.6%) reported climacturia and 7 agreed to undergo video-urodynamic evaluation (group 1), which was performed also in 5 controls (group 2). Those 12 men were also evaluated with 24-hour pad test, 5-item International Index of Erectile Function and International Prostate Symptom Score questionnaires. Results. Functional urethral length (FUL) was significantly lower in the climacturia group (P = 0.02) and time to continence recovery was significantly longer (P = 0.05). No other significant differences were found between the two groups. The radiological appearance of the vesicourethral junction at voiding cystourethrography was similar. Conclusions. To the best of our knowledge, this is the first functional and morphological evaluation of climacturia after RP. In our experience, this event is indirectly associated with a reduced FUL in the sphincter area, although both patients and controls were continent during daily activities. BNS technique seems to reduce time to continence recovery, although climacturic patients need longer time than control patients. Since in our series no rigidity of the vesicourethral anastomosis was radiographically evident, we believe that differences in FUL could explain OAI. Anatomical difference in membranous urethra length could explain the occurrence of this symptom in patients treated with the same surgical technique. Manassero F, Di Paola G, Paperini D, Mogorovich A, Pistolesi D, Valent F, and Selli C. Orgasm-associated incontinence (climacturia) after bladder neck-sparing radical prostatectomy: Clinical and video-urodynamic evaluation. J Sex Med 2012;9:2150–2156. Key Words. Climacturia, Orgasm-Associated Incontinence, Radical Prostatectomy, Urodynamic, Sexual Dysfunction Following Surgery for Prostate Cancer
J Sex Med 2012;9:2150–2156
© 2012 International Society for Sexual Medicine
Functional Evaluation of Climacturia after Pelvic Surgery Introduction
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ith improving surgical technique, nowadays, radical prostatectomy (RP) is a common urological procedure related to low incidence of postoperative morbidity, but high global number of late complications. Historically, urinary incontinence and erectile dysfunction are wellknown and partially accepted complications following RP with a reported rate of 21% and 39.4–56.9%, respectively [1]. In the last decade the quality of sexual life after RP especially concerning orgasm has been the object of the urologist’s attention [2,3]. Orgasm-Associated Incontinence (OAI) or climacturia (surgical complication grade I) [4] has been observed in male patients maintaining sexual potency after RP and cystectomy with neobladder reconstruction. It is more common than originally thought, and its incidence varies between 15.7% and 93% of cases when it is carefully looked for [5–7]. OAI is often not elicited by the treating physician, unlike urinary incontinence or erectile dysfunction, despite the impact that this problem can have on sexual life. In certain circumstances, small volumes of urine loss can have major impact on patients’ quality of life, leading to a great deal of anxiety and embarrassment or modifying sexual practices. The aim of our study was to evaluate from a functional point of view the bladder and the urethra in men with this recently reported postoperative symptom and to better understand its physiology. If it is inconvenient to perform video-urodynamics study during ejaculation, a possible pathogenesis of OAI could be identified comparing the results of the exam carried out in basal condition between climacturic and non-climacturic patients. Therefore, we investigated the prevalence and videourodynamic aspects of male urinary tracts in men who report climacturia, otherwise continent and potent after bladder neck-sparing (BNS) RP, and to the best of our knowledge, this is the first functional and morphological evaluation of bladders in men with this symptom. Material and Methods
Out of all the men who underwent BNS RP by a single surgeon during the period 2007–2009 and screened with a telephone interview, we identified 84 subjects suitable for participation in this study, since they were continent and potent with or without phosphodiesterase type 5 inhibitors at least
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1 year after BNS RP. The RP were carried out with careful dissection with scissors of the circular BN fibers in all patients, using the technique previously described [8]. Urinary continence, subjectively (telephone question) assessed and objectively (24hour pad test) confirmed, was defined as a leakage ⱕ2 g in 24 hours. Potency was defined as 5-item International Index of Erectile Function (IIEF-5) >22 points (out of 25). Climacturia was arbitrarily defined as at least three episodes of urinary leakage at the moment of climax, in patients otherwise completely continent, 1 year after surgery. Twenty-four patients out of 84 (28.6%) reported climacturia, and seven of them agreed to undergo video-urodynamic evaluation (group 1), which was performed also in five control patients (group 2), e.g., potent and continent men following BNS RP without climacturia. Those 12 men were also evaluated with a 24-hour pad test, IIEF-5 and International Prostate Symptom Score (IPSS) questionnaires. The study had been approved by the local Ethics Committee, and all patients signed the informed consent form. Video-urodynamics investigations were performed according to Good Urodynamic Practices/ International Continence Society using the MMS Solar EUREL unit (Eurel srl, Milan, Italy) [9]. Detailed urodynamic session included one initial uroflow with post-voiding residual (PVR), cystometry in a supine position, Valsalva Leak Point Pressure (VLPP) at 250 mL and maximum filling, urethral pressure profilometry with maximum urethral closure pressure (MUCP) and functional urethral length (FUL). The exam was performed with a 9 Fr double-lumen urethral catheter, filling the bladder with contrast material (mean filling rate of 50 mL/minute). Abdominal pressure was recorded using a 12 Fr intra-rectal balloon catheter. The static urethral pressure profile was estimated as well with the patient in the supine position, after cystometry, with bladder full, using a 9 Fr catheter with a mechanical arm at a rate of 1–2 mm/second. The catheter has a single transducer, and a slow steady perfusion rate of 2–10 mL/ minute is maintained during withdrawal of the catheter (Brown and Wickham technique) [10]. For radiological evaluation a digital system (FCR XG 5000 reader, Fujifilm, Fujifilm Corporation, Tokyo, Japan) was used. Contrast material was Visipaque (Iodixanol, GE Healthcare, Little Chalfont, United Kingdom; iodine concentration 320 mg/dL). Examinations were done by recording the urodynamic trace and, periodically, obtaining fluorosJ Sex Med 2012;9:2150–2156
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Table 1 Patient demographics and results of clinical and urodynamic tests, showing that the only two differences between climacturic group and control group are the reduced functional urethral length and the longer time to continence recovery in the first one Variable
Group 1 (7 cases) Mean-median (SD)
Group 2 (5 controls) Mean-median (SD)
P
Age at surgery (years) Gleason score IIEF-5 IPSS Q8 Capacity (mL) PVR (mL) Qmax (mL/second) Qmed (mL/second) VLPP (cm H2O) MUCP (cm H2O) FUL (mm) Time to continence (weeks)
64.1–65 6.4–7 22.3–22 6.3–3 1.1–1 475–500 0–0 21–20 8.7–7 93.3–100 60–58 20.3–20 21.1–26.1
61.8–62 6–6 22.2–22 4.2–4 0.8–1 435–450 0–0 26.2–26 14–14 113–105 98.8–96 35.2–35 0–0
0.48* 0.36* 0.93* 0.87* 0.67* 0.28* 0* 0.13* 0.09* 0.18* 0.15* 0.02* 0.02†
(3.89) (1.13) (1.11) (8.75) (1.06) (61.23) (0) (7.50) (3.72) (27.86) (24.71) (4.03) (16)
(5.31) (2.12) (1.30) (2.28) (0.83) (48.73) (0) (2.38) (3.53) (17.17) (44.13) (4.81) (0)
The statistical significance of differences between the two groups of patients was assessed through Wilcoxon rank sum test. The statistical difference between the two groups in time to continence was assessed through the log-rank test. All the analyses were performed using SAS v9.2 (SAS Institute Inc., Cary, NC, USA). *P value of Wilcoxon rank sum test †P value of log-rank test IIEF-5 = 5-item International Index of Erectile Function; IPSS = International Prostate Symptom Score; Q8 = IPSS question 8; PVR = post-voiding residual; VLPP = Valsalva Leak Point Pressure; MUCP = maximum urethral closure pressure; FUL = functional urethral length; SD = standard deviation
copy acquisitions in the presence of symptoms reported by the patient or alterations in the trace.
Statistical Analysis The distribution of the numerical variables among cases and controls were described by their mean ⫾ standard deviation and median. The statistical significance of differences between the two groups of patients was assessed through Wilcoxon rank sum test. The statistical difference between the two groups in time to continence was assessed through the log-rank test. P values < 0.05 were considered statistically significant. All the analyses were performed using SAS v9.2 (SAS Institute Inc., Cary, NC, USA). Results
The two groups were comparable for age at operation (median 65 vs. 62, mean 64.1 ⫾ 3.9 vs. 61.8 ⫾ 5.3 years), Gleason score (median 7 vs. 6, mean 6.4 ⫾ 1.1 vs. 6.0 ⫾ 2.1), a 24-hour pad test (median 0, mean 0), IIEF-5 scores (median 22, mean 22.3 ⫾ 1.1 vs. 22.2 ⫾ 1.3), IPSS (median 3 vs. 4, mean 6.3 ⫾ 8.7 vs. 4.2 ⫾ 2.3), and quality of life, measured by question 8 of IPSS (median 1, mean 1.1 ⫾ 1.1 vs. 0.8 ⫾ 0.8). In the climacturia group, the phenomenon began few months following the operation, at the sexual activity recovery, in almost all intercourses and persisted 1 year after surgery. Both patients and controls presented good bladder capacity (median J Sex Med 2012;9:2150–2156
500 vs. 450, mean 475 ⫾ 61.2 vs. 435 mL ⫾ 48.7) in absence of detrusor overactivity; maximum urinary flow rate (Qmax) at uroflowmetry was similar (median 20 vs. 26, mean 21.0 ⫾ 7.5 vs. 26.2 mL/second ⫾ 2.4) without PVR, as well as VLPP (median 100 vs. 105, mean 93.3 ⫾ 27.9 vs. 113 cmH2O ⫾ 17.2). The mean urinary flow rate (Qmed) was lower among patients with climacturia (7 vs. 14, mean 8.7 ⫾ 3.7 vs. 14 mL/second ⫾ 3.5, P = 0.09). The MUCP at the level of external sphincter was lower in the climacturia group (median 58 vs. 96, mean 60 ⫾ 24.7 vs. 98.8 cm H2O ⫾ 44.1), although not significant (P = 0.15), while FUL was significantly lower (median 20 vs. 35, mean 20.3 ⫾ 4.0 vs. 35.2 mm ⫾ 4.8; P = 0.02), as well as time to continence recovery, higher in the group 1 (median 26.1 vs. 0, mean 21.1 ⫾ 16.0 vs. 0 weeks ⫾ 0; P = 0.02). The observed data are reported in Table 1. The radiological appearance of the vesicourethral junction at voiding cystourethrography was similar in both groups: bladder neck looks relatively closed at rest and a regular opening of external sphincter without anastomotic strictures or rigidity at voiding phase (Figure 1). Discussion
The term of climacturia was introduced for the first time by Lee et al. in 2006 to describe “urine leakage at the moment of climax,” despite that already in 1996 Koeman et al. had described the symptom [11,12]. As well in 2006 the Cleveland group
Functional Evaluation of Climacturia after Pelvic Surgery
Figure 1 Regular radiological appearance of the vesicourethral junction at voiding cystourethrography in a climacturic patient, without difference with control group.
reported this new phenomenon calling it “ejaculatory urine incontinence,” highlighting that a few drops leakage during sexual intercourse could impair the quality of life. The year later Choi et al. implemented the definition with “orgasm associated incontinence” that with climacturia is the term with which it is presently known [13]. It is more common than originally thought when it is carefully looked for. Its incidence varies between 15.7% and 93% of cases depending on the definition used, how it is recorded (mail questionnaires, telephone interview, during physical evaluation), the type of radical surgery (prostatectomy vs. cystectomy, open or laparoscopic), and the duration of the symptom [5–7]. In a study of prevalence and nature of orgasmic dysfunctions after RP, Barnas et al. reported an incidence of incontinence associated with orgasm at any time after surgery in 93% of men, specifying that the leakage occurred always in 16%, occasionally in 44%, and rarely in 33% [6]. OAI occurs more frequently after RP than after radical cystectomy, and it is not related to the surgical technique (open vs. laparoscopic). More common within the first year after surgery, it is more likely to be reported in men complaining orgasmic pelvic pain and penile shortening [13,14]. Choi et al. failed to find an association
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with the extent of nerve-sparing, surgical margins, preoperative and postoperative sexual function, or daytime continence [13]. Although the pathophysiology of OAI has not been specifically studied and it is poorly understood, different explanations have been postulated. Orgasm combines pleasure and physiological changes at the moment of ejaculation. Immediately before orgasm, the internal sphincter with the bladder neck and the external sphincter are closed in unison, generating a high-pressure zone within the prostatic urethra. The ejaculation is the forcible expulsion of seminal contents from the urethral meatus due to the rhythmic contraction of pelvic-perineal musculature: the bladder neck is closed to prevent semen backflow into the bladder, the external sphincter opens suddenly and the high intraprostatic pressure combined with periurethral musculature contraction leads to antegrade sperm propulsion. As the accessory sex glands are removed at RP, these patients are unable to ejaculate, and thus they experience “dry orgasms.” In patients unable to effectively appose the bladder neck, retrograde ejaculation is common. Abouassaly et al. considered that it is probably also the case in patients who undergo RP, where urine can escape from the bladder and be propelled antegrade during ejaculation. This could be either a neurologic phenomenon or an anatomic one [15]. Intrinsic sphincter deficiency has been considered the primary cause of post-RP incontinence. It is attributable to malfunction of the distal urethral sphincter secondary to direct injury to the sphincter, its supporting structures or its neural innervation. However, daytime continence is not associated with OAI, suggesting a different mechanism. There is has a solid scientific reasoning behind this theory, since daily continence depends on external sphincter function, while OAI prevention depends on bladder neck function [13]. If the external urethral sphincter remains the dominant source of continence following RP, at the moment of climax with relaxation of the external urethral sphincter it could be reasonable that urine leakage would occur. Koeman et al. hypothesized that OAI was related to internal sphincter ablation during RP combined with relaxation of the external sphincter at orgasm [12]. What remains unclear with this hypothesis is why not all men after RP and some men after transurethral prostatic resection have climacturia: to our knowledge this has not been described. Lee et al.’s hypothesis is that bladder neck stricture or a J Sex Med 2012;9:2150–2156
2154 smaller caliber urethra would be less likely to leak urine, although their data do not support that bladder neck status and urethral caliber may have a role in determining climacturia [11]. Because orgasmic pain and loss of penile length have been associated with OAI, it is possible that the three dysfunctions have related mechanisms. Barnas et al. suggested that orgasmic pain following RP might be due to bladder neck spasm, similar to what is believed to occur in men with chronic pelvic pain disorder [6]. The assumption is that after RP physiological bladder neck closure at orgasm translates into spasm of the vesicourethral anastomosis, or pelvic floor musculature dystonia. The concept of bladder neck spasm is further enhanced by the success of the uroselective alphablocker tamsulosin for alleviating dysorgasmia [6,13]. Anorgasmia and decreased intensity of orgasm are most probably psychological events, presumably related to diagnosis of prostate cancer and major radical pelvic surgery [6,13]. Mulhall et al. postulated that cavernous nerve injury and the subsequent sympathetic hyperinnervation during autonomic nerve repair for competitive sprouting could be related to loss of penile length in the early stages after surgery. Assuming that the cavernous smooth muscle is highly contractile in response to adrenergic tone, sympathetic overdrive after cavernous nerve injury would result in a hypertonic condition and penile shortening. If the mechanisms underlying dysorgasmia and penile length loss are indeed sympathetically mediated, it is possible that OAI occurs by a similar process [14,16]. Another hypothesis is that a surgical technique that permits better preservation of the urethral sphincter and neurovascular bundles highly decreases the risk of having climacturia after RP [17,18]. Various mechanisms have been suggested, but none has been adequately tested. The present study was undertaken to better elucidate the pathophysiology of this phenomenon. Climacturia is infrequently spontaneously referred to by the patient who experienced it, but it should be investigated by the physician, even if it is very difficult to objectify. We selected patients completely continent in the daytime and potent to increase the reliability of their answers, and to identify the symptom “climacturia” alone. The incidence and prevalence of this condition are highly related to the definition used: we found a prevalence of 28.6% considering only continent and potent patient following RP. This percentage J Sex Med 2012;9:2150–2156
Manassero et al. could be lower considering all patients after radical surgery, but in our opinion only continent patients at the moment of the orgasm can experience this symptom, while the others easily do not recognize it or confuse it with other urine leakage. Mitchell et al. recently reported that the impact of RP on sexual quality of life is not driven exclusively by the return of erectile function, with a 12.1% of a major problem due to incontinence during sexual activity in sexually active men at 24 months [19]. The aim of our study was a morphological and functional evaluation of urinary tracts in men with this phenomenon more than its impact on quality of life. Moreover, there is no orgasm-specific questionnaire; there are numerous sexual function questionnaires, some too burdensome and complex for these type of patients, others designed for assessing erectile function before and after pharmacotherapy, more than assessing orgasmic function (IIEF-5). No differences in IPSS, IPSS question 8, and IIEF-5 emerged between cases and controls. Although both patients and controls were continent during daily activities, comparing the two groups, interestingly, we found statistically significant difference in FUL and in time to continence. Climacturic patients need also longer time to continence recovery compared with control patients, and they present a reduced FUL. Although the association was not statistically significant, climacturic patients presented a trend to have lower MUCP. Nevertheless, we know that anatomical difference in membranous urethra length could explain the occurrence of this symptom in patients treated with the same surgical technique. The part of membranous urethra and intact striated urethral sphincter that is left intact for anastomosis of bladder to urethra after RP may be important for reaching postoperative continence. Myers et al. showed that the external striated urethral sphincter, visually evident with magnetic resonance imaging (MRI), surrounds the urethral segment located between the prostate and the bulb and therefore they proposed the term “sphincteric urethra.” This unique muscular segment, known as membranous urethra, is mostly important for male urinary continence, and should be preserved at RP [20]. From the morphological point of view, neither a rigidity of the vesicourethral anastomosis nor other morphological appearances were radiographically evident in both groups that we studied, although this is a subjective evaluation. Cystoure-
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Functional Evaluation of Climacturia after Pelvic Surgery thrography is a dynamic examination, where the radiologist can appreciate eventual incomplete neck apposition, urethral strictures or anastomotic rigidity, but anatomical modifications of lower urinary tract after radical prostatic surgery do not allow univocal measurement. The trend toward lower MUCP, with the reduced FUL and the increased time to continence, seems to demonstrate that residual function of external sphincter may have a key role in understanding the physiology of this symptom: in climacturic patients the residual sphincter after RP, due either to anatomical differences of sphincteric/ membranous urethra or to surgeon ability to preserve urethral length, is enough for daytime continence, but not for continence at the moment of climax. We are aware of the limitations of the present study. The reduced number of cases and controls is related to the difficulties to convince otherwise healthy individuals to undergo invasive and embarrassing examination, which requires two catheters insertion and contrast bladder infusion. Moreover, the subjective reporting of this symptom by patients motivates our choice to perform the video-urodynamic exam in basal condition instead of during orgasm, not an easily documented and reproducible anatomical and psychological event. The proposal to perform the exam after intracavernous prostaglandin injection, to reproduce a similar situation, in our opinion is not valid because the mechanisms of erection are completely different from those of ejaculation.
The occurrence of this symptom in patients treated with the same surgical technique could be explained by anatomical difference in membranous urethra length, which direct measurement by MRI would represent a further point of interest. Corresponding Author: Francesca Manassero MD, PhD, Department of Urology, University of Pisa, via Paradisa 2, 56124 Pisa, Italy. Tel: +39-050-997745; Fax: +39-050-997745; E-mail: francy_manassero@ hotmail.com Conflict of Interest: None.
Statement of Authorship
Category 1 (a) Conception and Design Francesca Manassero; Davide Paperini; Cesare Selli (b) Acquisition of Data Francesca Manassero; Giuseppe Di Paola; Donatella Pistolesi (c) Analysis and Interpretation of Data Francesca Manassero; Andrea Mogorovich; Francesca Valent
Category 2 (a) Drafting the Article Francesca Manassero; Giuseppe Di Paola; Andrea Mogorovich; Francesca Valent (b) Revising It for Intellectual Content Francesca Manassero; Davide Paperini; Donatella Pistolesi; Cesare Selli
Category 3 Conclusions
Despite the limitation of a restricted number of patients, due to test invasiveness limiting recruitment, to the best of our knowledge, this is the first functional and morphological evaluation of male urinary tract in men reporting climacturia after RP and although these results can be regarded as preliminary, they remain innovative and should contribute to the better understanding of climacturia etiology. In our experience, this event is indirectly associated with a reduced FUL in the sphincter area, although both patients and controls were continent during daily activities. Indeed climacturic patients need longer time than control patients to continence recovery. Since in our series no rigidity of the vesicourethral anastomosis was radiographically evident, we believe that differences in FUL could be the cause of OAI.
(a) Final Approval of the Completed Article Francesca Manassero; Giuseppe Di Paola; Davide Paperini; Andrea Mogorovich; Donatella Pistolesi; Francesca Valent; Cesare Selli
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