Abstract
There is a paucity of published literature on the andrological consequences of urethral repair. Until recently authors have focused mainly on technical aspects and objective results. Reported outcomes of urethral reconstruction surgery have traditionally focused only on urodynamic parameters such as flow rates. Patient reported outcome measures have largely been neglected and there is a scarcity of well conducted systematic studies on the subject. For these reasons whether the different components of sexual life are more or less affected by different types of urethral reconstruction remains largely unknown. In an attempt to clarify the available scientific evidence, the authors make a critical review of available literature, systematizing it by sexual domain and study type. Brief pathophysiological correlations are discussed.
1. Introduction
Urethral stenosis, although relatively uncommon in the universe of urologic diseases, is by no means a rare condition. It accounts for about 52% of urethral and 1.8% of urologic pathology, respectively, and presents an estimated prevalence of 0.6% [1, 2]. Relatively young, active individuals are mostly affected. Its association with an unequivocal negative impact on the quality of life, whether resulting from the disease itself and its complications or whether consequence of the treatment(s) employed, is well established.
At present, there is no doubt that reconstructive surgery in the form of different types of urethroplasty represents the “gold standard” in the treatment of these patients. Urethroplasty is associated with reproductively high success rates, when properly employed. There is enough data in the literature regarding the results obtained with several techniques, anastomotic or substitution. When objective variables such as flow rates are considered, several authors describe success rates that exceed in many cases 80% whether for anterior urethra, bulbar [3–5] or penile [6–8], or whether for posterior urethra [9–11].
These data reflect however only one aspect of results, as patients carry out a substantially different perception of success than physicians, not only taking into account flow rates and radiological or endoscopic data. It is well known that there is a significant mismatch between what is considered a urethral reconstruction failure/success between treatment physicians and patients [12–14]. Aspects such as aesthetics or those related to sexual function are obviously important from the perspective of patients and often overlooked in the literature. If we do a simple exercise as, for example, an electronic search using the most widespread scientific literature database, PubMed, this disparity becomes obvious. If researches using terms like “urethroplasty and results” provide thousands of references, terms such as “urethral stenosis” or “urethroplasty” and “erectile dysfunction” or “impotence” result in only a few dozen scientific papers. Moreover, many books that specifically address urethral reconstruction almost exclusively focus on anatomical or technical aspects and there is a virtual absence of information about the andrological aspects of urethroplasty.
Although in recent years there has been a growing interest in relation to urethral stricture's andrologic implications, the relationship between urethroplasty and erectile dysfunction, for example, remains controversial up to the present day. The existence of few specific studies, heterogeneous study populations, differing methodologies, and diversity of procedures analyzed makes it very difficult to provide definitive answers.
Pathophysiology of Sexual Dysfunction. Surgical approaches involving the external genitalia have an unmistakable noxious potential in several domains of sexual function, aesthetic and dysmorphic changes.
Consequences in aesthetics and change of body image, mostly related to the distal urethroplasties, have obvious potential impact in terms of self-esteem and possibly sexual behavior. Although of subjective nature, these aspects are particularly noticeable in multioperated hypospadias patients, a group of patients of increasing importance in percentage terms that pose a particularly difficult approach.
Concerning erectile and ejaculatory dysfunction, potentially injured structures in the course of urethroplasty include several arterial structures, nerve branches (autonomic and/or somatic), and eventually myogenic components.
There is a recognized potential for injury of branches of the Common Penile Artery, essential in the hemodynamics of erection in posterior urethroplasties, and of more distal vessels, of smaller and questionable practical importance, in anterior urethroplasties.
Equally important are neurogenic autonomic lesions due to the proximity of the neurovascular bundles to the membranous urethra, potentially damaged in instrumentation of the posterior urethra [15, 16]. Somatic neurogenic components, either sensory or motor, involving the dorsal penile or perineal nerve and its branches, are also at risk, particularly during anterior urethroplasties [17–19].
Of potential functional importance, though debatable and still practically in the field of scientific curiosity, are the neuronal connections identified between autonomic and somatic pelvic, perineal, and even genital nerve terminals, making the latter capable of nitrergic activity. Authors like Yucel and Baskin [20] and Alsaid et al. [21] using immunohistochemistry-based studies in fetuses unequivocally demonstrate connections between the neurovascular bundles from the pelvic plexus, nitrergic, and components of the somatic nervous system (branches of the pudendal nerve such as the dorsal nerve of the penis and perineal nerve), giving them the capacity to release erectogenic mediators.
Finally, section and aggressive mobilization or denervation of the bulbospongiosus muscle to expose the bulbar urethra may result in more or less subtle changes in ejaculation dynamics, since the rhythmic contractions of the muscle during the expulsion phase are fundamental in seminal fluid expulsion [22–24].
2. Materials and Methods
A systematic review of several databases including PubMed, Cochrane Library, Embase, and Google Scholar was conducted. Systematic searches of these databases used terms as “urethroplasty,” “urethral reconstruction,” “urethral anastomosis,” “urethral stricture,” “urethral stenosis,” and “urethral obstruction,” and terms such as “erectile dysfunction,” “impotence,” “sexual dysfunction,” “ejaculatory dysfunction,” and “orgasmic dysfunction.” The search strategy used both keywords and MeSH terms and was limited to human studies.
The purpose of this study was to review the existing literature about the impact of urethroplasty in all domains of sexual function and to analyze it.
3. Results and Discussion
3.1. Body Image/Self-Esteem
Literature is absolutely lacking in terms of evaluation of the aesthetic consequences of urethroplasties performed in adulthood for urethral strictures. We can only infer conclusions based on findings from literature in the context of hypospadiology, a study population with necessarily different and very particular characteristics.
Despite all the limitations pointed out, there are a few studies that looked specifically at the cosmetic aspect of the reconstruction of the penile urethra in this context that allow us at least some critical reflections.
Authors as Bubanj et al. [25] used a postal questionnaire including questions about genitosexual functioning and sexual behavior in a comparative study of 37 patients submitted to urethroplasty for hypospadias repair 2–15 years earlier (mean age 27.8 ± 6.2 years/average number of surgeries 3.81 ± 3.37) and a group of 39 normal men (mean age 25.5 ± 5.3 years). No significant differences were found between the groups with regard to inhibition of search for sexual contacts or sexual relationship patterns. Participants in both groups were mostly satisfied with their body image (83,78% of patients with hypospadias versus 89.74% in the control arm). However, there were significant differences between the groups regarding the frequency of sexual activity and number of sexual partners. Only 51.35% of men with hypospadias regarded their sex life as fully satisfying against 76.92% of the control group.
Even et al. [26] analyzed a group of 15 young adult hypospadias patients (mean age 21.2 years) operated in childhood, employing instruments such as EuroQol 5, IIEF-15, and a nonvalidated questionnaire. One-third of patients thought that overall quality of life was distorted, although 80% were mostly satisfied with their sexual quality of life. The most important complaints were relative to the penile appearance.
Although subject to wide variation in individual perception, these aspects must of course be considered in addressing these patients and integrated with the other facets of the pathology/treatment strategy.
3.2. Erectile Dysfunction
3.2.1. Anterior Urethra: Prospective Studies
There are few prospective studies with correct methodology, making use of fully validated questionnaires such as the IIEF (International Index of Erectile Function) or the BMSFI (Brief Male Sexual Function Inventory) specifically dealing with anterior urethroplasties. Table 1 [27–31] lists these studies and the results obtained. It is evident that all these studies show statistical limitations. The small sample size by itself can obscure statistically significant differences simply as a consequence of underpowered studies. In fact, none of the studies makes explicit reference to calculations in order to define a minimum sample size that would be required to show 5 to 10% difference in outcomes for example. Although with relatively small samples and relatively short follow-up, the overwhelming majority of studies did not find statistically significant degradation of erectile function after urethroplasty compared to baseline.
Table 1.
Authors, year | n | Questionnaire | Follow-up (months) | Age (median) | Results |
---|---|---|---|---|---|
Sharma et al., 2011 [27] | 34 | BMSFI | 3 | 34,6 | Preop BMSFI: 10,21; postop: 10,34 P = 0,554, NSD |
| |||||
Anger et al., 2007 [28] | 25 | IIEF | 6,2 | 39 | Preop IIEF: 62,6; postop: 59,6 P = 0,29, NSD |
| |||||
Dogra et al., 2011 [29] | 78 | IIEF-5 | 15,5 | 38,1 | 38% of postop ED “96% recovery by 6 months,” NSD |
| |||||
Raber et al., 2005 [30] | 30 | IIEF | 51 | 42 | Preop IIEF5: 24 ± 8,7; postop, 24,8 ± 4,96 P = 0,77, NSD |
| |||||
Erickson et al., 2010 [31] | 52 | IIEF | 7,2 | 40,6 | Preop IIEF5: 18,7; postop:12,6 P < 0,0001: SSD “90% of postop ED recovered by 6 months” |
IIEF: International Index of Erectile Function; BMSFI: Brief Male Sexual Function Inventory; NSD: no statistical difference; SSD: statistically significant difference.
The only discordant study is from Erickson et al. [31]. These authors analyze prospectively 52 men with penile or bulbar urethral stenosis subjected to several types of urethroplasties (penile urethra: ventral onlay or inlay, 2-stage; bulbar urethra: end-to-end anastomotic or augmented anastomotic repair). Patients were evaluated serially every 3 to 6 months by the IIEF. De novo erectile dysfunction (ED) was defined as an IIEF decrease of at least 5 points and recovery as a score less than 2 points from baseline. Although ED was observed in 38% of patients, 90% of these were found to recover function in accordance with established criteria, with an average recovery time of 190 days.
3.2.2. Anterior Urethra: Retrospective Studies
Table 2 [32–38] summarizes the available retrospective studies that used structured, validated, or nonvalidated questionnaires. Being retrospective, these studies already have inherent limitations in terms of methodology. Additional obvious limitations in terms of sample size in most of them and the frequent use of nonvalidated questionnaires add additional limitations in terms of produced scientific evidence. Moreover, unfortunately these are recurrent limitations in the reconstructive urethral surgery scientific literature.
Table 2.
Authors, year | n | Questionnaire | Follow-up (months) | Age (median) | Results |
---|---|---|---|---|---|
Singh et al., 2010 [32] | 150 | BMSFI | >3 | 40 | Mean preop BMSFI EF: 9,1; postop: 8,8 P = 0,39, NSD |
| |||||
Erickson et al., 2007 [33] | 52 | BMSFI | 22,3 | 41,7 | Mean preop BMSFI EF: 9,2; postop: 8,8 P = 0,11, NSD |
| |||||
Coursey et al., 2001 [34] | 174 | NVQ | 36 | 43,8 | 69,1% no difference in erectile function 30,9% worsened erectile function |
| |||||
Nelson et al., 2005 [35] | 11 | IIEF | 56,4 | 30,6 | 0% ED |
| |||||
Morey and Kizer, 2006 [36] | 22 | NVQ | 26,1 | 39,95 | No difference between end-to-end and extended anastomotic techniques or other types of penile surgery |
| |||||
Welk and Kodama, 2012 [37] | 44 | NVQ | 40 | 27,6 | No difference between nontransecting APA and dorsal graft |
| |||||
Ekerhult et al., 2013 [38] | 169 | NVQ | 12–132 | 16–75 | No difference between anastomotic repair and onlay |
IIEF: International Index of Erectile Function; ED: erectile dysfunction; BMSFI: Brief Male Sexual Function Inventory; NSD: no statistical difference; NVQ: nonvalidated questionnaire.
Other studies [39–41] are available, although with debatable statistical quality, making it difficult to draw any valid conclusions. Data reported are mainly descriptive and the presence of preoperative ED was not uniformly reported. Often the presence of postoperative ED was asserted only by means of a simple question [39–41]. These series have focused above all on technical aspects and success rates, and ED was only briefly referred to. ED rates ranged from 0 [40] to 7% [41].
Concerning the studies included in Table 2, it is apparent that there is some disparity regarding the employed methodology and the way results are presented. Authors like Singh et al. [32] and Erickson et al. [33] present a methodology perfectly intelligible and easy to read. These authors evaluated a cohort of patients submitted to different types of anterior urethroplasties using the same questionnaire. In both cases no statistically significant differences were found concerning the 3 specific questions related to erectile function of the BMFSI. For its part, Coursey et al. [34], perhaps in one of the first published papers specifically on the subject, report a 30.9% rate of degradation of erections after a mean follow-up of 36 months. It is interesting however that the authors used as a control group patients undergoing circumcision in which they found reduction in erectile performance in 27.3%, with no significant differences between the two groups. On the other hand, Morey and Kizer [36] Welk and Kodama [37] and Ekerhult et al. [38] are mainly series in which two techniques or technical variants (end-to-end, extended anastomotic, or onlay graft urethroplasty) are analyzed. There was no difference in the ED occurrence among the techniques. In all groups, reported ED rates were small.
3.2.3. Other Prospective Studies: Anterior and Posterior Urethra
There are 3 additional prospective studies, presented in Table 3, involving mixed cohorts of patients undergoing anterior and posterior urethroplasties [42–44]. All used the IIEF-5 as assessment method. With follow-ups in the range of 6 to 27 months, no significant differences were found between pre- and postoperative scores by any of the authors.
Table 3.
Authors, year | n | Study type | Questionnaire | Follow-up (months) | Age (median) | Results |
---|---|---|---|---|---|---|
Lumen et al., 2011 [42] | 20 | P | IIEF-5 | 6 | 48 | Mean preop IIEF5: 15; postop: 11,62 P = 0,11,NSD |
| ||||||
Xie et al., 2009 [43] | 125 | P |
IIEF-5 SLQQ |
27,3 | ? |
Mean preop IIEF5: 16,57; postop: 17,22 “significant decrease in EEIF-5 at 3 months but not at 6 months” |
| ||||||
Johnson and Latini, 2011 [44] | 37 | P | IIEF-5 | 9 | 45 | Mean preop IIEF5: 15; postop: 10 P = 0,39,NSD |
IIEF: International Index of Erectile Function; SLQQ: Sexual Life Quality Questionnaire; ED: erectile dysfunction; BMSFI: Brief Male Sexual Function Inventory; NSD: no statistical difference; P: prospective.
3.2.4. Posterior Urethra
Lesions of the posterior urethra, associated with the overwhelming majority of cases to traumatic injuries of the pelvic ring, are unequivocally linked to erectile dysfunction, either by direct damage to neurovascular structures or by indirect action of edema, inflammation, and fibrosis. Presence of urethral trauma in pelvic fractures is a widely documented risk factor of erectile dysfunction. 42% of patients with pelvic fracture and urethral lesions had ED compared with only 5% of patients with fractures and without urethral injury [45]. The literature accounts for ED percentages ranging from 18% or less to 72% [46], although the relative roles of the traumatic event and potential iatrogeny induced by reconstructive surgery remain unclear. Aspects such as lack of consensus on the definition of ED, heterogeneous series regarding the severity of the trauma, and obvious discrepancies in the evaluation methods explain the variability of results. The potential of spontaneous recovery up to about 24 months after the traumatic event is also widely documented, probably related to neuropraxia recovery and development of accessory vessels after vascular trauma. For this reason, the timing of the evaluation in relation to trauma and surgery plays an important role in result variability, since studies that report ED with evaluation 3–15 months after trauma present rates of ED significantly elevated (60–72%), when compared with series in which this evaluation was made at least 2 years after the traumatic event (18–32%) [46].
Table 4 is intended to summarize the existing literature on the subject [9, 10, 47–57]. It is quite apparent that the overwhelming majority of the series did not make use of validated questionnaires in the evaluation of patients and the evaluation methodology in relation to erectile function is, at most, only briefly mentioned. If trauma plays an obvious role in the etiology of ED, it is much harder to distinguish the specific role played by reconstructive surgery. Many of the studies only report global rates of ED after reconstruction and, as such, potentially encompass the effects of trauma and surgical iatrogenesis, more or less ameliorated by the aforementioned spontaneous recovery. Studies that specifically evaluate erectile function before and after urethroplasty are thereby especially enlightening.
Table 4.
Authors, year | n | Study type | Questionnaire | Follow-up (years) | Age (median) | Results |
---|---|---|---|---|---|---|
Anger et al., 2009 [47] | 26 | R | IIEF | 4,4 | 40,2 | 54% ED 31% severe ED |
| ||||||
Corriere, 2001 [48] | 60 | R | ? | 27,3 | 35 | 33% “complete” ED |
| ||||||
Shenfeld et al., 2003 [49] | 25 | D | — | <3 | 28,6 | 72% preoperative ED |
| ||||||
Koraitim, 2005 [10] | 155 | R | — | 1–22 | 21 | 34% “definitive” ED 2% after surgery |
| ||||||
Mundy, 1996 [9] | 82 | R | ? | >5 | ? | 7% “permanent” ED |
| ||||||
Yin et al., 2011 [50] | 76 | R | — | 42,5 | 34,5 | 95% remained potent 5% de novo ED 59% recovered potency |
| ||||||
Lumen et al., 2009 [51] | 61 | R | — | 5,58 | 34 | 32,8% ED previous to surgery 2 cases spontaneous recovery |
| ||||||
Onen et al., 2005 [52] | 49 | R | NVQ | 12 | 20 | 18,4% ED at last follow-up |
| ||||||
Mouraviev et al., 2005 [53] | 96 | R | — | 8,8 | ? | 34% after realignment 42% after delayed repair |
| ||||||
Tunç et al., 2000 [54] | 58 | R | — | 3,9 | 24,2 | 16,2% de novo ED |
| ||||||
Aboutaieb et al., 2000 [55] | 35 | R | — | ? | 25 | 18,3% ED early repair 5,3% ED delayed repair |
| ||||||
Morey and Mcaninch, 1997 [56] | 82 | R | — | >1 | ? | 54% ED previous to repair 38% ED after repair |
| ||||||
Corriere et al., 1994 [57] | 50 | R | — | >1 | ? | 48% ED previous to repair 32% ED after repair |
IIEF: International Index of Erectile Function; NVQ: nonvalidated questionnaire; ED: erectile dysfunction; P: prospective; R: retrospective; D: descriptive.
Koraitim [10] analyzed a series of 155 patients who suffered posterior urethral trauma, although, without using any validated tool and not specifying the definition of ED used, the author refers to the fact that, of previously potent patients before trauma, 40% became impotent. Of the 66 patients without ED before urethroplasty only 2 were impotent as a result of surgery, in both cases after surgeries of great technical complexity, exceeding 9 hours. On the other hand, 29 of 44 previously impotent patients recovered erectile function after urethroplasty.
Analyzing 76 patients with a follow-up ranging from 14 to 74 months, Yin et al. [50] report an ED rate of 42% after trauma. Of the 58% of potent patients, 95% remained potent after urethroplasty and 5% developed de novo ED. 59% of impotent patients after trauma recovered erectile function after surgery.
Tunç et al. [54] described a series of 77 patients with posterior urethra injury treated with deferred urethroplasty after suprapubic diversion. 25.8% of the evaluated patients developed ED after trauma. Erectile function was evaluated prior to surgery through clinical history in 58 patients. Of the previously potent patients, de novo ED occurred in 16.2%. The authors make reference to an impotent patient that recovered erectile function after surgery.
Morey and Mcaninch [56] and Corriere Jr. et al. [57] on the other hand report important rates of recovery of erectile function in impotent patients after posterior urethroplasty. A decrease in impotency rates of 54 to 38% and from 48 to 32%, respectively, was observed. No de novo ED was reported in both studies after urethroplasty.
Finally, we can make use of a subanalysis of six studies specifically dealing with posterior urethroplasties, analyzing erectile function before and after urethroplasty, encompassed in a broader meta-analysis, discussed later [58]. After elimination of one of the studies in order to improve heterogeneity and thus improve the statistical quality, The analysis reveals advantage for postsurgical status (24,01% versus 43,27%; OR 2,51; 95% CI: 1,82–3,45; P < 0,001).
With the limitations already mentioned, posterior urethroplasty does not seem to play a significant deleterious effect per se on erectile function. The overwhelming majority of these patients have ED prior to surgery and surgical reconstruction might even be beneficial in a subgroup of these patients. Aspects such as removal of fibrosis and scar tissue, essential from a technical point of view to achieve a successful urethroplasty, could lead to decompression of nerve structures and allow recovery of function. Restoration of micturition and the simple removal of a suprapubic catheter, allowing improvement of psychological aspects and self-image, may also play a role in this regard.
3.2.5. Meta-Analysis
Two fairly recent meta-analysis sought to systematize the available studies and shed some light on the subject (Table 5) [58–60].
Table 5.
Meta-analyses | Studies | n | Urethroplasty | Results |
---|---|---|---|---|
Feng et al. [58] | 23 | 1729 | Anterior and posterior urethroplasty | No significant difference before or after urethroplasty [OR 0,85; 95% CI (0,52–1,40); P = 0,53] ED incidence after posterior urethroplasty lower than before [24,01% versus 43,27%; OR 2,51; 95% CI (1,82–3,45); P < 0,01] No significant difference before or after penile urethroplasty [23,53% versus 35,29%; CI (0,13–2,52); P = 0,45] No significant difference between penile and bulbar urethroplasty [23,81% versus 16,67% OR 1,62; 95% CI: 0,51–5,81, P = 0,41] ED incidence after graft urethroplasty significantly lower than anastomotic urethroplasty [(OR 0,32; 95% CI: 0,11–0,93; P = 0,04)] |
| ||||
Blaschko et al. [60] | 36 | 2323 | Anterior urethroplasty | 1% incidence of de novo ED after urethroplasty ED transient and resolved between 6 and 12 months in 86% of cases No statistical significant association between de novo ED and stricture location, mean stricture length, number of previous instrumentations/repairs, or type of repair |
Feng et al. [58] examined 790 studies of which only 23 met the predefined inclusion criteria (randomized controlled trial (RCT) and cohort studies), corresponding to 1729 patients undergoing anterior and posterior urethroplasties. Five of these studies globally analyzed erectile function before and after urethroplasty and found no significant differences between pre- and postoperative scores [OR 0.85; 95% CI (0,52–1,4); P = 0,53]. The authors conducted several subanalyses. According to the location of the stenosis, a single study compared the incidence of ED before and after penile urethroplasty specifically and found no statistically significant differences (23.53% versus 35.29%, P = 0,45). Only two studies compared penile with bulbar substitution urethroplasties and also found no significant differences in erectile scores (23.81% versus 16.67% OR 1.62; 95% CI: 0.51 to 5.81, P = 0,41). These same two studies allowed comparison of buccal mucosa substitution urethroplasties with anastomotic end-to-end urethroplasties revealing lower ED rates for substitution versus anastomotic (OR 0.32; 95% CI: 0.11 to 0.93; P = 0,04). Finally only one study analyzed ED occurrence before and after bulbar end-to-end urethroplasty; no statistically significant differences were found (24.14% versus 27.59%; P = 0,76). Regarding posterior urethra, the meta-analysis analyzes aspects such presence versus absence of surgical history, immediate repair versus deferred repair, and primary alignment versus immediate repair; all have discarded statistically significant differences.
In turn Blaschko et al. [60] analyzed studies related to the last 15 years in English language, covering only anterior urethroplasties carried out in adulthood, specifically looking for the occurrence of ED as a consequence of urethroplasty. Of the 736 identified articles, 36 met the inclusion criteria, including 2323 patients who were subject to statistical analysis. De novo ED incidence varied between 0 and 38%, and generally it was a very rare occurrence, 1% (CI 1–3). The incidence of de novo ED did not increase when patients were directly asked about erectile function [OR 0.83 (CI 0.06 to 10.90)] and there was no association with the location or mean stricture length, type of repair, or number of previous failed instrumentation, urethrotomies or urethroplasties. In the overwhelming majority of cases de novo ED resolved spontaneously 6–12 months after surgery; 7 of the 21 studies that have registered the occurrence of de novo ED also reported occurrence of ED resolution in 86% (50/58) of cases. There was substantial heterogeneity in the studies (I-squared = 93%, P < 0,001), attributable in part to the variation in how ED was reported.
In summary, the limitations already mentioned obviously make it impossible to provide complete definitive answers regarding the relationship between urethroplasty and erectile dysfunction. Although it is unwise to assume that there is no relationship (in particular when dealing with any individual patient), globally, the evidence accumulated to date, encompassing progressive methodological and statistical quality, seems to point only to a small deleterious role for either anterior or posterior urethroplasty.
3.3. Ejaculatory Dysfunction
Table 6 summarizes the studies that address the impact of various types of urethroplasty in ejaculatory function [3, 27, 32, 33, 61–63]. Although most of the studies are retrospective and merely assessed the presence of anterograde ejaculation, most used validated instruments, ejaculatory domains of MSHQ or BMFSI.
Table 6.
Authors, year | n | Study type | Questionnaire | Follow-up (months) | Urethroplasty | Age (median) | Results |
---|---|---|---|---|---|---|---|
Singh et al., 2010 [32] | 150 | R | BMSFI | >3 | AU | 40 | Mean preop BMSFI Ej: 4,7; postop: 6,3 P < 0,001, improved |
| |||||||
Sharma et al., 2011 [27] | 34 | P | BMSFI | 3 | AU | 34,6 | Mean preop BMSFI Ej: 4,68; postop: 6,71 P = 0,00, improved |
| |||||||
Erickson et al., 2007 [33] | 52 | R | BMSFI | 4 | AU | 41,7 | Mean preop BMSFI Ej: 5,3; postop: 6,2 P < 0,04, improved |
| |||||||
Barbagli et al., 2008 [3] | 60 | R | N. Valid. | 68 | AU∗ | 39 | 23% ejaculatory dysfunction |
| |||||||
Erickson et al., 2010 [61] | 43 | P | MSHQ | 6,8 | AU | 40,4 | Mean preop MSHQ Ej: 25,54; postop: 26,94 P = 0,17, NSD overall 70% no change 19% improved 11% decreased |
| |||||||
El-Assmy et al., 2015 [62] | 58 | R | MSHQ | 61,3 | PU | 31,6 | 8,6 ejaculatory dysfunction |
| |||||||
Anger et al., 2008 [63] | 32 | R | N. Valid. | 58,8 | PU | 38,6 | 100% antegrade ejaculation 15,6% decreased volume |
BMSFI: Brief Male Sexual Function Inventory; MSHQ: Male Sexual Health Questionnaire; AU: anterior urethroplasty; ∗100% end-to-end anastomosis; NSD: no statistical difference.
Most authors comparing pre- and postoperative scores report significant improvement in ejaculatory function [27, 32, 33]. This result is perfectly understandable, given the considerable improvement in urethral caliber achieved, resulting in better expulsive capacity of the seminal fluid. Authors like Erikson et al. [61] although not finding overall statistically significant differences between pre- and postoperative scores refer to statistically significant improvements in men with ejaculatory dysfunction preoperatively.
Authors as Barbagli et al. [3] identified ejaculatory dysfunction after anastomotic urethroplasty in the form of decreased ejaculatory flow or need for urethral milking surpassing 20%, so that some caution is needed when analyzing these results.
In order to minimize this potential problem, several authors have proposed some minimally invasive procedures in an attempt to maximally preserve structures involved in ejaculatory mechanics. Authors like Barbagli and Kulkarni [23, 24] present approaches referred to as “muscle and nerve sparing urethroplasty” or “one sided urethroplasty,” which aim to minimize the potential iatrogeny over the bulbospongiosus muscle or its innervation. Advantages from these technical refinements remain thus far in the field of theoretical or anatomophysiological hypothesis. Results obtained were not disclosed and as such these approaches lack appropriate validation in this specific context.
3.4. Orgasmic Dysfunction
Two studies evaluated this component of sexuality in the context of urethroplasty (Table 7) [28, 35]. In both cases the orgasmic domain was analyzed together with the other domains of IIEF. Both works refer to case series with less than 20 patients on various circumstances, urethroplasty for hypospadias and bulbar urethroplasty. None of the authors found any negative influence of urethroplasty on orgasmic function.
Table 7.
Authors, year | n | Study type | Questionnaire | Follow-up (months) | Urethroplasty | Age (median) | Results |
---|---|---|---|---|---|---|---|
Anger et al., 2007 [28] | 25 | P | IIEF | >3 | AU | 39 | Mean preop IIEF (orgasmic domain): 8,6; postop: 8,3 P = 0,28, NSD |
| |||||||
Nelson et al., 2005 [35] | 11 | R | IIEF | 56,4 | Hypospadias | 30,6 | No change “All patients experienced orgasm” |
IIEF: International Index of Erectile Function; AU: anterior urethroplasty; NSD: no statistical difference.
Although a virtual absence of literature on the subject makes it difficult to draw any critical analysis on the subject, a lack of influence of urethral surgery on orgasm is not surprising, since orgasm is essentially considered a neurophysiological phenomenon [64].
3.5. Fertility
There are some specific articles that address fertility in the context of urethroplasty (Table 8) [52, 63, 65]. These studies essentially describe the seminal parameters of patients having undergone posterior urethroplasty. There is no reference to cases of azoospermia. Of course it is impossible to implicate the surgical procedure with these findings, although the relationship does not seem obvious. Anyway, due to the high prevalence of male factor infertility in the general population, it is impossible to draw any conclusion.
Table 8.
Authors, year | n | Study type | Follow-up (months) | Urethroplasty | Age (median) | Results |
---|---|---|---|---|---|---|
Anger et al., 2008 [63] | 13 | D | >3 | PU | 38,6 | 46% normal (WHO) 53% oligospermia 8% asthenozoospermia 30% oligozoospermia |
| ||||||
Iwamoto et al., 1992 [65] | 14 | D | 56,4 | PU | ? | 50% normal (WHO) 21% oligozoospermia 35% asthenozoospermia |
| ||||||
Onen et al., 2005 [52] | 19 | D | 144 | PU | 20 | 26,3% abnormal semen parameters (WHO) |
D: descriptive; R: retrospective; PU: posterior urethroplasty.
4. Conclusions
Although there are a lot of series describing the results achieved with various types of urethroplasties, the andrological aspects of this pathology and its treatment(s) are clearly insufficiently studied. The available literature is confusing, dispersed, not systematized, and often containing methodological deficits. Although we have been assisting in recent efforts in an attempt to obtain more and better data, there are still obvious gaps that prevent valid conclusions on the subject. Large scale, prospective investigations using standardized validated questionnaires are needed to reliably elucidate the real impact of urethroplasty on the different domains of sexual function.
Conflict of Interests
The author declares that there is no conflict of interests regarding the publication of this paper.
References
- 1.Romero P., Mora A. Reseñas históricas sobre el tratamiento de la estenosis uretral. Actas Urológicas Españolas. 1993;17(3):159–161. [PubMed] [Google Scholar]
- 2.Santucci R. A., Joyce G. F., Wise M. Male urethral stricture disease. Journal of Urology. 2007;177(5):1667–1674. doi: 10.1016/j.juro.2007.01.041. [DOI] [PubMed] [Google Scholar]
- 3.Barbagli G., Guazzoni G., Lazzeri M. One-stage bulbar urethroplasty: retrospective analysis of the results in 375 patients. European Urology. 2008;53(4):828–833. doi: 10.1016/j.eururo.2008.01.041. [DOI] [PubMed] [Google Scholar]
- 4.Pansadoro V., Emiliozzi P., Gaffi M., Scarpone P. Buccal mucosa urethroplasty for the treatment of bulbar urethral strictures. The Journal of Urology. 1999;161(5):1501–1503. doi: 10.1016/s0022-5347(05)68938-0. [DOI] [PubMed] [Google Scholar]
- 5.Wessells H. Ventral onlay graft techniques for urethroplasty. Urologic Clinics of North America. 2002;29(2):381–387. doi: 10.1016/s0094-0143(02)00029-0. [DOI] [PubMed] [Google Scholar]
- 6.Dubey D., Kumar A., Mandhani A., Srivastava A., Kapoor R., Bhandari M. Buccal mucosal urethroplasty: a versatile technique for all urethral segments. BJU International. 2005;95(4):625–629. doi: 10.1111/j.1464-410x.2005.05352.x. [DOI] [PubMed] [Google Scholar]
- 7.Fichtner J., Filipas D., Fisch M., Hohenfellner R., Thuroff J. W. Long-term outcome of ventral buccal mucosa onlay graft urethroplasty for urethral stricture repair. Urology. 2004;64(4):648–650. doi: 10.1016/j.urology.2004.05.011. [DOI] [PubMed] [Google Scholar]
- 8.Dubey D., Sehgal A., Srivastava A., Mandhani A., Kapoor R., Kumar A. Buccal mucosal urethroplasty for balanitis xerotica obliterans related urethral strictures: the outcome of 1 and 2-stage techniques. Journal of Urology. 2005;173(2):463–466. doi: 10.1097/01.ju.0000149740.02408.19. [DOI] [PubMed] [Google Scholar]
- 9.Mundy A. R. Urethroplasty for posterior urethral strictures. British Journal of Urology. 1996;78(2):243–247. doi: 10.1046/j.1464-410X.1996.11617.x. [DOI] [PubMed] [Google Scholar]
- 10.Koraitim M. M. On the art of anastomotic posterior urethroplasty: a 27-year experience. The Journal of Urology. 2005;173(1):135–139. doi: 10.1097/01.ju.0000146683.31101.ff. [DOI] [PubMed] [Google Scholar]
- 11.Kizer W. S., Armenakas N. A., Brandes S. B., Cavalcanti A. G., Santucci R. A., Morey A. F. Simplified reconstruction of posterior urethral disruption defects: limited role of supracrural rerouting. The Journal of Urology. 2007;177(4):1378–1382. doi: 10.1016/j.juro.2006.11.036. [DOI] [PubMed] [Google Scholar]
- 12.Kessler T. M., Fisch M., Heitz M., Olianas R., Schreiter F. Patient satisfaction with the outcome of surgery for urethral stricture. Journal of Urology. 2002;167(6):2507–2511. doi: 10.1016/s0022-5347(05)65015-x. [DOI] [PubMed] [Google Scholar]
- 13.Voelzke B. B. Critical review of existing patient reported outcome measures after male anterior urethroplasty. The Journal of Urology. 2013;189(1):182–188. doi: 10.1016/j.juro.2012.08.096. [DOI] [PubMed] [Google Scholar]
- 14.Jackson M. J., N'Dow J., Pickard R. The importance of patient-reported outcome measures in reconstructive urology. Current Opinion in Urology. 2010;20(6):495–499. doi: 10.1097/mou.0b013e32833cf4a5. [DOI] [PubMed] [Google Scholar]
- 15.Schwalenberg T., Neuhaus J., Liatsikos E., Winkler M., Löffler S., Stolzenburg J.-U. Neuroanatomy of the male pelvis in respect to radical prostatectomy including three-dimensional visualization. BJU International. 2010;105(1):21–27. doi: 10.1111/j.1464-410x.2009.08702.x. [DOI] [PubMed] [Google Scholar]
- 16.Costello A. J., Brooks M., Cole O. J. Anatomical studies of the neurovascular bundle and cavernosal nerves. BJU International. 2004;94(7):1071–1076. doi: 10.1111/j.1464-410x.2004.05106.x. [DOI] [PubMed] [Google Scholar]
- 17.Yucel S., Baskin L. S. Neuroanatomy of the male urethra and perineum. BJU International. 2003;92(6):624–630. doi: 10.1046/j.1464-410x.2003.04435.x. [DOI] [PubMed] [Google Scholar]
- 18.Akman Y., Liu W., Li Y. W., Baskin L. S. Penile anatomy under the pubic arch: reconstructive implications. Journal of Urology. 2001;166(1):225–230. doi: 10.1016/s0022-5347(05)66131-9. [DOI] [PubMed] [Google Scholar]
- 19.Baskin L. S., Erol A., Li Y. W., Liu W. H. Anatomy of the neurovascular bundle: is safe mobilization possible? Journal of Urology. 2000;164(3, part 2):977–980. doi: 10.1016/s0022-5347(05)67230-8. [DOI] [PubMed] [Google Scholar]
- 20.Yucel S., Baskin L. S. Identification of communicating branches among the dorsal, perineal and cavernous nerves of the penis. The Journal of Urology. 2003;170(1):153–158. doi: 10.1097/01.ju.0000072061.84121.7d. [DOI] [PubMed] [Google Scholar]
- 21.Alsaid B., Moszkowicz D., Peschaud F., et al. Autonomic-somatic communications in the human pelvis: computer-assisted anatomic dissection in male and female fetuses. Journal of Anatomy. 2011;219(5):565–573. doi: 10.1111/j.1469-7580.2011.01416.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Yang C. C., Bradley W. E. Reflex innervation of the bulbocavernosus muscle. BJU International. 2000;85(7):857–863. doi: 10.1046/j.1464-410X.2000.00560.x. [DOI] [PubMed] [Google Scholar]
- 23.Barbagli G., De Stefani S., Annino F., De Carne C., Bianchi G. Muscle- and nerve-sparing bulbar urethroplasty: a new technique. European Urology. 2008;54(2):335–343. doi: 10.1016/j.eururo.2008.03.018. [DOI] [PubMed] [Google Scholar]
- 24.Kulkarni S., Barbagli G., Sansalone S., Lazzeri M. One-sided anterior urethroplasty: a new dorsal onlay graft technique. BJU International. 2009;104(8):1150–1155. doi: 10.1111/j.1464-410x.2009.08590.x. [DOI] [PubMed] [Google Scholar]
- 25.Bubanj T. B., Perovic S. V., Milicevic R. M., Jovcic S. B., Marjanovic Z. O., Djordjevic M. M. Sexual behavior and sexual function of adults after hypospadias surgery: a comparative study. The Journal of Urology. 2004;171(5):1876–1879. doi: 10.1097/01.ju.0000119337.19471.51. [DOI] [PubMed] [Google Scholar]
- 26.Even L., Bouali O., Moscovici J., et al. Long-term outcomes after hypospadias surgery: sexual reported outcomes and quality of life in adulthood. Journal of Progress in Urology. 2015;25(11):655–664. doi: 10.1016/j.purol.2015.04.006. [DOI] [PubMed] [Google Scholar]
- 27.Sharma V., Kumar S., Mandal A. K., Singh S. K. A study on sexual function of men with anterior urethral stricture before and after treatment. Urologia Internationalis. 2011;87(3):341–345. doi: 10.1159/000330268. [DOI] [PubMed] [Google Scholar]
- 28.Anger J. T., Sherman N. D., Webster G. D. The effect of bulbar urethroplasty on erectile function. The Journal of Urology. 2007;178(3):1009–1011. doi: 10.1016/j.juro.2007.05.053. [DOI] [PubMed] [Google Scholar]
- 29.Dogra P. N., Saini A. K., Seth A. Erectile dysfunction after anterior urethroplasty: a prospective analysis of incidence and probability of recovery—single-center experience. Urology. 2011;78(1):78–81. doi: 10.1016/j.urology.2011.01.019. [DOI] [PubMed] [Google Scholar]
- 30.Raber M., Naspro R., Scapaticci E., et al. Dorsal onlay graft urethroplasty using penile skin or buccal mucosa for repair of bulbar urethral stricture: results of a prospective single center study. European Urology. 2005;48(6):1013–1017. doi: 10.1016/j.eururo.2005.05.003. [DOI] [PubMed] [Google Scholar]
- 31.Erickson B. A., Granieri M. A., Meeks J. J., Cashy J. P., Gonzalez C. M. Prospective analysis of erectile dysfunction after anterior urethroplasty: incidence and recovery of function. Journal of Urology. 2010;183(2):657–661. doi: 10.1016/j.juro.2009.10.017. [DOI] [PubMed] [Google Scholar]
- 32.Singh U. P., Maheshwari R., Kumar V., Srivastava A., Kapoor R. Impact on sexual function after reconstructive surgery for anterior urethral stricture disease. Indian Journal of Urology. 2010;26(2):188–192. doi: 10.4103/0970-1591.65384. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Erickson B. A., Wysock J. S., McVary K. T., Gonzalez C. M. Erectile function, sexual drive, and ejaculatory function after reconstructive surgery for anterior urethral stricture disease. BJU International. 2007;99(3):607–611. doi: 10.1111/j.1464-410X.2006.06669.x. [DOI] [PubMed] [Google Scholar]
- 34.Coursey J. W., Morey A. F., McAninch J. W., et al. Erectile function after anterior urethroplasty. The Journal of Urology. 2001;166(6):2273–2276. doi: 10.1016/s0022-5347(05)65549-8. [DOI] [PubMed] [Google Scholar]
- 35.Nelson C. P., Bloom D. A., Kinast R., Wei J. T., Park J. M. Patient-reported sexual function after oral mucosa graft urethroplasty for hypospadias. Urology. 2005;66(5):1086–1089. doi: 10.1016/j.urology.2005.05.057. [DOI] [PubMed] [Google Scholar]
- 36.Morey A. F., Kizer W. S. Proximal bulbar urethroplasty via extended anastomotic approach—what are the limits? Journal of Urology. 2006;175(6):2145–2149. doi: 10.1016/s0022-5347(06)00259-x. [DOI] [PubMed] [Google Scholar]
- 37.Welk B. K., Kodama R. T. The augmented nontransected anastomotic urethroplasty for the treatment of bulbar urethral strictures. Urology. 2012;79(4):917–921. doi: 10.1016/j.urology.2011.12.008. [DOI] [PubMed] [Google Scholar]
- 38.Ekerhult T. O., Lindqvist K., Peeker R., Grenabo L. Low risk of sexual dysfunction after transection and nontransection urethroplasty for bulbar urethral stricture. Journal of Urology. 2013;190(2):635–638. doi: 10.1016/j.juro.2013.02.075. [DOI] [PubMed] [Google Scholar]
- 39.Eltahawy E. A., Virasoro R., Schlossberg S. M., McCammon K. A., Jordan G. H. Long-term followup for excision and primary anastomosis for anterior urethral strictures. The Journal of Urology. 2007;177(5):1803–1806. doi: 10.1016/j.juro.2007.01.033. [DOI] [PubMed] [Google Scholar]
- 40.Dubey D., Sehgal A., Srivastava A., Mandhani A., Kapoor R., Kumar A. Buccal mucosal urethroplasty for balanitis xerotica obliterans related urethral strictures: the outcome of 1 and 2-stage techniques. The Journal of Urology. 2005;173(2):463–466. doi: 10.1097/01.ju.0000149740.02408.19. [DOI] [PubMed] [Google Scholar]
- 41.Ortega J. L. L., Peña C. P. Surgical treatment of urethral stenosis. Results of 100 urethroplasties. Archivos Espanoles de Urologia. 2009;62(2):109–114. doi: 10.4321/s0004-06142009000200004. [DOI] [PubMed] [Google Scholar]
- 42.Lumen N., Spiers S., De Backer S., Pieters R., Oosterlinck W. Assessment of the short-term functional outcome after urethroplasty: a prospective analysis. The International Brazilian Journal of Urology. 2011;37(6):712–718. doi: 10.1590/s1677-55382011000600005. [DOI] [PubMed] [Google Scholar]
- 43.Xie H., Xu Y.-M., Xu X.-L., Sa Y.-L., Wu D.-L., Zhang X.-C. Evaluation of erectile function after urethral reconstruction: a prospective study. Asian Journal of Andrology. 2009;11(2):209–214. doi: 10.1038/aja.2008.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Johnson E. K., Latini J. M. The impact of urethroplasty on voiding symptoms and sexual function. Urology. 2011;78(1):198–201. doi: 10.1016/j.urology.2011.01.045. [DOI] [PubMed] [Google Scholar]
- 45.King J. Impotence after fractures of the pelvis. The Journal of Bone & Joint Surgery—American Volume. 1975;57(8):1107–1109. [PubMed] [Google Scholar]
- 46.Koraitim M. M. Predictors of erectile dysfunction post pelvic fracture urethral injuries: a multivariate analysis. Urology. 2013;81(5):1081–1085. doi: 10.1016/j.urology.2012.12.040. [DOI] [PubMed] [Google Scholar]
- 47.Anger J. T., Sherman N. D., Dielubanza E., Webster G. D. Erectile function after posterior urethroplasty for pelvic fracture-urethral distraction defect injuries. BJU International. 2009;104(8):1126–1129. doi: 10.1111/j.1464-410X.2009.08589.x. [DOI] [PubMed] [Google Scholar]
- 48.Corriere J. N., Jr. 1-Stage delayed bulboprostatic anastomotic repair of posterior urethral rupture: 60 patients with 1-year followup. Journal of Urology. 2001;165(2):404–407. doi: 10.1097/00005392-200102000-00012. [DOI] [PubMed] [Google Scholar]
- 49.Shenfeld O. Z., Kiselgorf D., Gofrit O. N., Verstandig A. G., Landau E. H., Pode D. The incidence and causes of erectile dysfunction after pelvic fractures associated with posterior urethral disruption. The Journal of Urology. 2003;169(6):2173–2176. doi: 10.1097/01.ju.0000067660.51231.05. [DOI] [PubMed] [Google Scholar]
- 50.Yin L., Li Z., Kong C., et al. Urethral pull-through operation for the management of pelvic fracture urethral distraction defects. Urology. 2011;78(4):946–950. doi: 10.1016/j.urology.2011.05.027. [DOI] [PubMed] [Google Scholar]
- 51.Lumen N., Hoebeke P., Troyer B. D., Ysebaert B., Oosterlinck W. Perineal anastomotic urethroplasty for posttraumatic urethral stricture with or without previous urethral manipulations: a review of 61 cases with long-term followup. The Journal of Urology. 2009;181(3):1196–1200. doi: 10.1016/j.juro.2008.10.170. [DOI] [PubMed] [Google Scholar]
- 52.Onen A., Öztürk H., Kaya M., Otçu S. Long-term outcome of posterior urethral rupture in boys: a comparison of different surgical modalities. Urology. 2005;65(6):1202–1207. doi: 10.1016/j.urology.2005.01.039. [DOI] [PubMed] [Google Scholar]
- 53.Mouraviev V. B., Coburn M., Santucci R. A. The treatment of posterior urethral disruption associated with pelvic fractures: comparative experience of early realignment versus delayed urethroplasty. The Journal of Urology. 2005;173(3):873–876. doi: 10.1097/01.ju.0000152145.33215.36. [DOI] [PubMed] [Google Scholar]
- 54.Tunç H. M., Tefekli A. H., Kaplancan T., Esen T. Delayed repair of post-traumatic posterior urethral distraction injuries: long-term results. Urology. 2000;55(6):837–841. doi: 10.1016/s0090-4295(00)00464-7. [DOI] [PubMed] [Google Scholar]
- 55.Aboutaieb R., Sarf I., Dakir M., et al. Surgical treatment of traumatic ruptures of the posterior urethra. Progres en Urologie. 2000;10(1):58–64. [PubMed] [Google Scholar]
- 56.Morey A. F., Mcaninch J. W. Reconstruction of posterior urethral disruption injuries: outcome analysis in 82 patients. The Journal of Urology. 1997;157(2):506–510. doi: 10.1016/s0022-5347(01)65188-7. [DOI] [PubMed] [Google Scholar]
- 57.Corriere J. N., Jr., Rudy D. C., Benson G. S., Coburn M., Diamond D. L., McAninch J. W. Voiding and erectile function after delayed one-stage repair of posterior urethral disruptions in 50 men with a fractured pelvis. The Journal of Trauma. 1994;37(4):587–589. doi: 10.1097/00005373-199410000-00011. [DOI] [PubMed] [Google Scholar]
- 58.Feng C., Xu Y.-M., Barbagli G., et al. The relationship between erectile dysfunction and open urethroplasty: a systematic review and meta-analysis. Journal of Sexual Medicine. 2013;10(8):2060–2068. doi: 10.1111/jsm.12181. [DOI] [PubMed] [Google Scholar]
- 59.Sangkum P., Levy J., Yafi F. A., Hellstrom W. J. Erectile dysfunction in urethral stricture and pelvic fracture urethral injury patients: diagnosis, treatment, and outcomes. Andrology. 2015;3(3):443–449. doi: 10.1111/andr.12015. [DOI] [PubMed] [Google Scholar]
- 60.Blaschko S. D., Sanford M. T., Cinman N. M., McAninch J. W., Breyer B. N. De novo erectile dysfunction after anterior urethroplasty: a systematic review and meta-analysis. BJU International. 2013;112(5):655–663. doi: 10.1111/j.1464-410x.2012.11741.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Erickson B. A., Granieri M. A., Meeks J. J., McVary K. T., Gonzalez C. M. Prospective analysis of ejaculatory function after urethral reconstruction. Journal of Urology. 2010;184(1):238–242. doi: 10.1016/j.juro.2010.03.038. [DOI] [PubMed] [Google Scholar]
- 62.El-Assmy A., Benhassan M., Harraz A. M., Nabeeh A., Ibrahiem E. H. I. Ejaculatory function after anastomotic urethroplasty for pelvic fracture urethral injuries. International Urology and Nephrology. 2015;47(3):497–501. doi: 10.1007/s11255-015-0923-2. [DOI] [PubMed] [Google Scholar]
- 63.Anger J. T., Sherman N. D., Webster G. D. Ejaculatory profiles and fertility in men after posterior urethroplasty for pelvic fracture-urethral distraction defect injuries. BJU International. 2008;102(3):351–353. doi: 10.1111/j.1464-410x.2008.07657.x. [DOI] [PubMed] [Google Scholar]
- 64.Stoléru S., Fonteille V., Cornélis C., Joyal C., Moulier V. Functional neuroimaging studies of sexual arousal and orgasm in healthy men and women: a review and meta-analysis. Neuroscience and Biobehavioral Reviews. 2012;36(6):1481–1509. doi: 10.1016/j.neubiorev.2012.03.006. [DOI] [PubMed] [Google Scholar]
- 65.Iwamoto T., Yajima M., Yamagoe M., Kuroko K., Inoue T., Osada T. Fertility in patients after surgical repair of membranous urethral strictures associated with pelvic fractures. Japanese Journal of Urology. 1992;83(4):505–511. doi: 10.5980/jpnjurol1989.83.505. [DOI] [PubMed] [Google Scholar]