Muscle- and Nerve-sparing Bulbar Urethroplasty: A New Technique

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1 available at journal homepage: Surgery in Motion Muscle- and Nerve-sparing Bulbar Urethroplasty: A New Technique Guido Barbagli a, Stefano De Stefani b, Filippo Annino b, *, Cosimo De Carne b, Giampaolo Bianchi b a Center for Reconstructive Urethral Surgery, Arezzo, Italy b Department of Urology, University of Modena-Reggio Emilia, Modena, Italy Article info Article history: Accepted March 7, 2008 Published online ahead of print on March 24, 2008 Keywords: Urethra Urethroplasty Bulbospongiosum muscle Perineal nerve Central tendon of the perineum Abstract Background: To describe a new surgical technique for the repair of bulbar urethral strictures to preserve the bulbospongiosum muscle and its perineal innervation. Objective: Surgical steps of muscle- and nerve-sparing bulbar urethroplasty are described. The outcome is provided regarding semen sequestration and postvoiding dribbling. Design, Setting, and Participants: We performed the procedure in 12 patients (average age: yr) with bulbar urethral strictures (average stricture length: 4.47 cm). Surgical Procedure: Six patients underwent urethroplasty using a ventral oral mucosal onlay graft, and six patients underwent urethroplasty using a dorsal oral mucosal onlay graft. In all patients, the surgical approach to the bulbar urethra was made avoiding dissection of the bulbospongiosum muscle from the corpus spongiosum and leaving the central tendon of the perineum intact. Measurements: Clinical outcome was considered a failure when any postoperative instrumentation was needed. The primary outcome examined the technical feasibility of the muscle- and nerve-sparing bulbar urethroplasty. The secondary outcome examined the presence or absence of postoperative postvoid dribbling and semen sequestration using a nonvalidated questionnaire (Appendix). Results and Limitations: In all patients, postoperative voiding cystourethrography was performed 3 wk after surgery and no urethral sacculation was evident. Urethrography were repeated after 6 mo and 12 mo. postvoid dribbling or semen sequestration was demonstrated in all patients at 6 mo and 12 mo after surgery. patient showed stricture recurrence. The average follow-up was mo (range 12 mo to 26 mo, median 13.5 mo). Conclusions: Bulbar urethroplasty preserving the bulbospongiosum muscle, the central tendon of the perineum, and the perineal nerves is a safe, feasible, minimally invasive alternative to traditional bulbar urethroplasty. # 2008 European Association of Urology. Published by Elsevier B.V. All rights reserved. * Corresponding author. Department of Urology, University of Modena-Reggio Emilia, L.go del Pozzo, 71, Modena, Italy. Tel ; Fax: address: f_annino@hotmail.com (F. Annino) /$ see back matter # 2008 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi: /j.eururo

2 Introduction 2. Patients and methods Urethral sacculation causes postvoiding dribbling, which is a natural complication of any kind of unsupported graft or flap anterior substitution urethroplasty. The mechanical weakening of the unsupported grafted area is evident on postoperative voiding cystourethrography because retrograde urethrography may fail to show urethral sacculation [1]. Surprisingly, the clinical evidence of postvoiding dribbling may also occur in patients who underwent bulbar urethroplasty but who also showed a normal voiding cystourethrography [1]. In 2005, we decided to include a nonvalidated telephone questionnaire (Appendix) in our follow-up study to investigate the prevalence of postoperative sexual and urinary dysfunction following one-stage anastomotic or substitution bulbar urethroplasty. In 60 of 153 patients who underwent bulbar endto-end anastomosis, 12 patients (20%) experienced decreased force of semen emission; for 2 patients (3.3%), ejaculation was possible only by manually compressing the perineum at the level of the urethral bulb [2]. In 67 of 210 patients who underwent one-stage substitution urethroplasty using oral mucosal grafts, 20 patients (29.8%) showed decreased force of the semen emission; 34 patients (50.7%) showed some degree of postvoiding dribbling (unpublished data). Fortunately, these minor postoperative dysfunctions did not modify the overall satisfaction of the surgery, and this optimistic patient evaluation is also probably influenced by the good outcome obtained with the regard to urinary function [2]. Moreover, postvoid dribbling and semen sequestration will likely be a postoperative complication following any bulbar urethroplasty [2]. The surgical approach to reach the bulbar urethra includes extensive dissection of the bulbospongiosum muscle, and sectioning of the central tendon of the perineum is suggested for proximally located bulbar strictures. Recently, we suggested the hypothesis that in some patients, postvoid dribbling and loss of semen emission could be caused by neural damage to the bulbospongiosum (bulbocavernosus) muscle or to the perineal nerves during their dissection in preparation of the bulbar urethra [1,2]. In this article, we describe a new oral mucosal onlay graft bulbar urethroplasty that preserves the bulbospongiosum muscle, the central tendon of the perineum, and the perineal nerves to reduce the risk of postvoiding dribbling and loss of semen emission, thus improving patient quality of life following bulbar urethroplasty Patient population Twelve patients with an average age of yr (range: 37 to 69 yr, median 40.5 yr) underwent bulbar urethroplasty using an oral mucosal graft while preserving the bulbospongiosum muscle and the central tendon of the perineum. Preoperative evaluation included clinical history, physical examination, urine culture, residual urine measurement, uroflowmetry, urethral ultrasound, and retrograde and voiding cystourethrography. The stricture etiology was previous urethral instrumentation in five cases (41.66%) and unknown in seven cases (58.33%). Patients with lichen sclerosis or failed hypospadias repair were excluded. Stricture length was 3 to 4 cm in five patients (41.7%), 4 to 5 cm in four patients (33.3%), and 5 to 6 cm in three patients (25%). The average stricture length was 4.47 cm (range: 3 to 6 cm, median 4.45 cm). Ten patients (83.3%) had undergone dilation or internal urethrotomy before referral to our center Surgical techniques Six patients underwent urethroplasty using a ventral oral mucosal onlay graft, and six patients underwent urethroplasty using a dorsal oral mucosal onlay graft. The dorsal location of the graft was selected for long distal strictures, whereas the ventral graft location was selected for shorter proximal strictures. The patient is placed in a simple lithotomy position. The patient s calves are carefully placed in Allen stirrups with sequential inflatable compression sleeves, and the lower extremities are then suspended by the patient s feet within the boots of the stirrups. Proper positioning ensures that there is no pressure on any aspect of the calf muscles and no inward boot rotation so as to avoid perineal nerve injury. The skin of the suprapubic region, scrotum, and perineum is shaved, and this region is prepared and draped appropriately. The oral mucosal graft is harvested from the cheek according to the standard technique [3] Ventral oral mucosal onlay graft urethroplasty Methylene blue is injected into the urethra to better define the urethral mucosa. A midline perineal incision is made. The bulbospongiosum muscle is separated from the corpus spongiosum of the bulbar urethra using delicate, smooth scissors, leaving the lateral margins of the muscle and the central tendon of the perineum intact (Fig. 1A). The muscle is pulled down using two small Farabeuf retractors, and the ventral urethral surface is fully exposed (Fig. 1B). The distal extent of the stenosis is identified, the corpus spongiosum is incised along the ventral midline, and the urethral lumen is fully exposed (Fig. 1C). The stricture is then incised along its entire length by extending the urethrotomy distally and proximally. Once the entire stricture has been incised, the length and width of the remaining urethral plate are measured. The oral mucosal graft is trimmed to its appropriate size according to

3 337 Fig. 1 Ventral oral mucosal onlay graft urethroplasty: (A) The bulbospongiosum muscle is separated from the corpus spongiosum leaving the lateral margins of the muscle and the central tendon of perineum intact. (B) The bulbospongiosum muscle is pulled down, exposing the ventral urethral surface. (C) The corpus spongiosum is opened along the midline, and the ventral urethral surface is fully exposed. (D) The oral mucosal graft is sutured to the proximal and distal apices and to the left margin of the urethral mucosal plate. (E) The graft is rotated and sutured to the right margin of the mucosal urethral plate. (F) The corpus spongiosum is closed over the graft, and fibrin glue is injected over the corpus spongiosum. (G) The bulbospongiosum muscle is picked up to cover the corpus spongiosum.

4 338 Fig. 2 Dorsal oral mucosal onlay graft urethroplasty: (A) The bulbar urethra is dissected from the corpora cavernosa, leaving the bulbospongiosum muscle and the central tendon of the perineum intact. (B) The urethra is rotated 180 degrees, and the dorsal urethral surface is fully opened. (C) The urethra is moved to the right side, and fibrin glue is injected over the corpora cavernosa. (D) The graft is fixed over the fibrin glue bed. (E) The distal and proximal apices of the graft are sutured to the apices of the urethrotomy. (F) The urethra, with the intact bulbospongiosum muscle, is rotated to cover the graft. (G) The graft is covered by the urethra, and fibrin glue is injected over the urethra.

5 339 the length and width of the urethrotomy. The two ends of the graft are sutured to the proximal and distal apices of the urethrotomy, and running 6-0 polyglactin suture is used to complete a watertight anastomosis between the left margin of the graft and the left margin of the urethral mucosal plate (Fig. 1D). A Foley 16-French grooved silicone catheter is inserted. The graft is rotated over the catheter, and running 6-0 polyglactin suture is used to complete a watertight anastomosis between the right margin of the graft and the right margin of the mucosal urethral plate (Fig. 1E). After completion of graft suturing, the corpus spongiosum is closed over the graft with 4-0 polyglactin interrupted suture and 2 ml of fibrin glue are injected over the corpus spongiosum (Fig. 1F). The bulbospongiosum muscle is picked up to cover the spongiosum tissue (Fig. 1G). Colles fascia, the perineal fat, and the skin are closed with interrupted absorbable sutures. The catheter is left in place for 3 wk Dorsal oral mucosal onlay graft urethroplasty Methylene blue is injected into the urethra to better define the urethral mucosa. A midline perineal incision is made. The bulbar urethra is dissected from the corpora cavernosa starting from the distal tract where muscles are absent, leaving the bulbospongiosum muscle and the central tendon of the perineum intact (Fig. 2A). The urethra is rotated 180 degrees, the distal extent of the stenosis is identified, the dorsal urethral surface is incised along the midline, and the urethral lumen is exposed (Fig. 2B). The stricture is then incised along its entire length by extending the urethrotomy distally and proximally. Once the entire stricture has been incised, the length and width of the remaining urethral plate is measured. The oral mucosal graft is trimmed to an appropriate size according to the length and width of the urethrotomy. The bulbar urethra is moved to the right side, and 2 ml of fibrin glue are injected over the albuginea of the corpora cavernosa (Fig. 2C) [4]. The oral mucosal graft is fixed over the fibrin glue bed (Fig. 2D) [4]. The two apices of the graft are sutured to the proximal and distal apices of the urethrotomy (Fig. 2E). A Foley 16-French grooved silicone catheter is inserted. The bulbar urethra, with the intact bulbospongiosum muscle, is rotated to its original position over the graft (Fig. 2F). Three interrupted 4-0 polyglactin sutures for each side are used to stabilize the urethral margins to the corpora cavernosa over the graft. At the end of the procedure, the graft is completely covered by the urethra, then by the muscles, and 2 ml of fibrin glue are injected over the urethra to prevent urinary leakage (Fig. 2G) [4]. Colles fascia, the perineal fat, and the skin are closed with interrupted absorbable sutures. The catheter is left in place for 3 wk Postoperative care and follow-up criteria The patient ambulates on the first postoperative day and is discharged from the hospital 3 d after surgery. All patients receive postoperative broad-spectrum antibiotics and are maintained on oral antibiotics until the catheter is removed. Three weeks after surgery, the bladder is filled with contrast medium, the Foley catheter is removed, and voiding cystourethrography is obtained. Six and 12 mo after surgery, the prevalence of postoperative sexual and urinary dysfunction were investigated using a nonvalidated questionnaire (Appendix). 3. Results The mean operative time was 90 min (range 80 to 110 min). intraoperative or postoperative complications were observed. Clinical outcome was considered a failure when any postoperative instrumentation was needed, including dilation. In all patients, postoperative voiding cystourethrography was performed 3 wk after surgery and no urinary leakage was present. Uroflowmetry and urine culture were repeated every 4 mo in the first year and annually thereafter. When symptoms of decreased force of stream were present and uroflowmetry was less than 14 ml/sec, urethrography, urethral ultrasound, and urethroscopy were repeated. The average follow-up was mo (range 12 to 26 mo, median 13.5 mo). patient showed stricture recurrence or urethral sacculation on voiding urethrography. With regard to the prevalence of postoperative ejaculation disorders and postvoiding dribbling, investigated using the nonvalidated telephone questionnaire, no patient showed decreased force of semen emission or postvoiding dribbling at 6 mo and 12 mo after surgery. Of six patients, none declared that he was dissatisfied with the outcome of the surgery. 4. Discussion The corpus spongiosum of the urethra, the bulbospongiosum muscle, and their functioning are rarely fully investigated. The bulbospongiosum muscle is a striated muscle located in the perineum, wrapped around the big bulb of the urethra. Its function is to propel seminal fluid during ejaculation. In 1962, the original studies of Kollberg et al established this muscle as primarily responsible for ejaculation [5]. Rhythmic contractions of the bulbospongiosum muscle and other perineal muscles expel semen from the urethra and probably have an important role in expelling urine, avoiding urine sequestration in the large urethral bulb following micturition. The pudendal nerve is the major somatic pathway of the male genitalia, which consists of three major branches: the dorsal nerve of the penis, the inferior rectal nerve, and the perineal nerve [6]. The dorsal nerve of the penis is primarily a sensory

6 340 nerve, and its role in male sexual function is well defined [6]. The perineal nerve is one of the three branches of the pudendal nerve that innervates the pelvic floor and its structures [6]. The motor portions of the nerve also innervate the bulbospongiosum and ischiocavernosus muscles, which contract in response to sexual stimulation [6]. The sensory portion of the perineal nerve is distributed to the skin of the perineum, scrotum, and ventral aspect of the penis (frenulum area) [6]. Bulbospongiosum muscle contraction is elicited by stimulation of the dorsal nerve of the penis and following stimulation of the perineal nerve [5]. Yang and Bradley illustrated the role of the perineal nerve in bulbospongiosum muscle contractions and suggested that ejaculatory disorders may result from disruption of one or more of the reflex pathways providing innervation of the bulbospongiosum muscle [7]. These disorders may manifest as decreased force of semen expulsion and low semen volume caused by inefficient bulbospongiosum contractility [7]. Yucel and Baskin reported that perineal nerves innervate the bulbospongiosum muscle and send fine branches that penetrate the corpus spongiosum, mainly in the bulbar area [8]. Moreover, these authors showed that branches of the dorsal nerve of the penis at the junction of the corpus cavernous and corpus spongiosum assemble into a network with the perineal nerves [8]. According to the neuroanatomy of the male urethra and perineum, described by Yucel and Baskin, the perineal nerves are easily injured during bulbar urethroplasty performed according to the standard procedures [8,9]. Moreover, sometimes the muscles could be damaged by the retractor branches (see Fig. 3). This kind of damage definitely involves the nerves and compromises the muscle function. In this case, the suture of the muscles cannot restore the damaged nerves and muscles fibers. During dissection of the central tendon of the perineum, the perineal nerves may likely be damaged upon emergence from the ischiorectal fossa or, when the bulbospongiosum muscle is fully divided along the midline, the fine branches of the perineal nerves penetrating into the corpus spongiosum may be damaged (Fig. 4). Moreover, the perineal nerve branches may be damaged by incorrect or excessive use of a cautery. In our preliminary experience with preservation of the bulbospongiosum muscle, perineal nerves, and the central tendon of the perineum in bulbar urethral reconstruction, the short-term results on this limited series of patients were satisfactory. Consequently, we have extended the use of this technique to an adjunctive series of patients who Fig. 3 Operating field after standard bulbar urethroplasty: The bulbospongiosum muscle is clearly damaged on both sides laterally. This damage is determined during the dissection of the muscles from the urethral bulb and by the retractor branches. It is evident that the main fibers of the nerves (laterally) as well as the fine branches going into the bulb of the urethra (medially) are both destroyed. Even if we could try to reconstruct the muscles, their function will never be restored. underwent urethroplasty for proximal bulbar urethral strictures or posterior urethroplasty (unpublished data for short-term follow-up). ne of the patients included in the present study showed urethral sacculation at voiding urethrography; consequently, in our cases, urethral sacculation is not responsible for postvoiding dribbling. Higher rigidity of the reconstructed urethra is not the cause of postvoiding dribbling and loss of semen emission because the bulbospongiosum muscle is mainly responsible for urethral contraction and not the urethra by itself (as clearly demonstrated by some studies reported in the literature) [5 8]. Further comparative studies on a large and homogeneous series of patients are necessary to confirm that the preservation of nervous and muscular structures involved in the mechanism of expelling urine and semen from the big bulb of the urethra is really beneficial compared to the standard procedures described for bulbar urethroplasty. In patients with postoperative postvoiding dribbling associated with semen sequestration or loss of semen emission, the surgeon suggests

7 341 and surgical suggestions to improve the short- and long-term outcomes and minimize the risk of postoperative complications [16]. 5. Conclusions Fig. 4 Injury of the perineal nerves during a standard bulbar urethroplasty: The perineal nerves may likely be damaged at their emergence from the ischiorectal fossa or when the bulbospongiosum muscle is divided along the midline (red outline). using manual emptying of the bulbar urethra after micturition or semen emission. Moreover, in younger patients, semen sequestration or loss of the semen emission may compromise fertility. These postoperative complications still represent unsatisfactory outcomes following any kind of bulbar urethroplasty, and we are engaged in improving our surgical techniques to improve the quality of life of our patients. Recently, Eltahawy et al presented a new, vessel-sparing excision and primary anastomosis of the urethra, preserving the arteries of the bulb [10]. In the future, all types of urethroplasty should be more anatomic and conservative when possible. At present, patients with a simple urethra stricture have a 90% success rate [2], which decreases to 80% in patients with complex urethral stricture disease [1]. Instead, the success rate for patients with congenital disease involving genitalia and urethra (failed hypospadias repair) does not exceed 70%, and 30% of these patients may require multiple, repeated surgeries to recover from urethra micturition [11 15]. As urologists involved in the treatment of urethral stricture diseases, the challenge is to make room from a new urethral science, collecting the right clinical, radiological, Reconstructive urethral surgery requires technical refinement. Preservation of the perineal muscles and nerves represents a slight but significant step toward perfecting the surgical technique of bulbar urethral reconstruction using a minimally invasive approach. Longer follow-up on a larger series of patients is necessary to confirm our satisfactory preliminary reports of this technique, which preserves the nervous and muscular structures involved in the mechanism of expelling urine and semen from the bulbar urethra. We are still working on gathering data. Author contributions: Filippo Annino had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Barbagli. Acquisition of data: Annino, De Carne. Analysis and interpretation of data: Barbagli, De Stefani. Drafting of the manuscript: Barbagli. Supervision: Bianchi. Other (specify): Video Annino, De Carne; Buccal mucosa harvesting De Stefani Financial disclosures: I certify that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: Dr Montorsi receives honoraria from Pfizer, Johnson & Johnson, and Siemens. Dr Pierce is a paid consultant to EU International. Funding/Support and role of the sponsor: ne. Appendix A. Supplementary data The Surgery in Motion video accompanying this article can be found, in the online version, at doi: /j.eururo and via Subscribers to the printed journal will find the Surgery in Motion DVD enclosed.

8 342 Appendix B. nvalidated Telephone Questionnaire Changes in ejaculation Did you complain of ejaculation disorders after the surgery? Did you recognize changes in ejaculation after the surgery in comparison with your previous status? Does ejaculation occur with a difficult stream? If yes, what is the stream like? stream Very poor spontaneous stream The stream occurs only by manually compressing the perineum. Is the ejaculation difficulty present: Always Sometimes Seldom Did difficult ejaculation cause negative changes in your relationship with your partner? Did you have children after the surgery? Neurovascular penile disorders Did you complain of penile erection disorders after the surgery? Does your glans swell fully during erection? If no: The glans does not swell. The glans swell only partially. The glans is fully swollen at the beginning of erection but does not maintain full swelling throughout sexual activity. Did you have negative changes in your sexual activity as a result this problem? If yes, what kind of problems were you aware of? Psychological problems Problems during vaginal intercourse Other minor problems Did you recognize a change in penile sensitivity after surgery? If yes, where did you notice these changes in sensitivity? In the glans In the penile skin In the distal penile shaft In the entire penile shaft What was penile sensitivity like after surgery? Decreased Increased t specifically altered Did penile sensitivity change in relation to: Touch Cold or heat All stimuli During erection, do you experience cold glans? Did you experience negative changes in your sexual activity as a result of this problem? If yes, what kind of problems were you aware of? Psychological problems Problems during vaginal intercourse Other minor problems Changes in urinary function Did you experience postvoiding dribbling? If yes, how much leakage did you experience? One or two drops A few drops Many drops Did you notice any urine spots on your underwear or trousers? If yes, did it happen: Infrequently Often Very often Did you use pads? If yes, how many pads did you use? One per day Three per day Three or more per day At the end of the voiding phase, did you manipulate the urethra or perineum to complete emptying? Using this behavior, can you avoid postvoiding dribbling? Final assessment of surgery Are you satisfied with the surgical outcome and what is your judgment of the final results? 1 t satisfied, negative 2 Poor satisfaction, poor 3 Satisfied, good 4 Very satisfied, excellent If your answer above was number 1 or 2: Is it because there was no improvement in urinary function? Is it because sexual activity worsened?

9 343 Appendix B. (Continued ) Would you repeat the surgery? If no, why not? Because of postoperative pain Because of psychological problems Because the outcome was different from what I expected References [1] Barbagli G, Palminteri E, Guazzoni G, Montorsi F, Turini D, Lazzeri M. Bulbar urethroplasty using buccal mucosa grafts placed on the ventral, dorsal or lateral surface of the urethra: Are results affected by the surgical technique? J Urol 2005;174: [2] Barbagli G, De Angelis M, Romano G, Lazzeri M. Long-term follow up of bulbar end-to-end anastomosis: a retrospective analysis of 153 patients in a single center experience. J Urol 2007;178: [3] Markiewicz MR, Margarone III JE, Barbagli G, Scannapieco FA. Oral mucosa harvest: an overview of anatomic and biologic considerations. EAU-EBU Update Series 2007; 5: [4] Barbagli G, De Stefani S, Sighinolfi MC, Annino F, Micali S, Bianchi G. Bulbar urethroplasty with dorsal onlay buccal mucosal graft and fibrin glue. Eur Urol 2006;50: [5] Yang CC, Bradley WE. Somatic innervation of the human bulbocavernosus muscle. Clinical Neurophysiology 1999;110: [6] Uchio EM, Yang CC, Kromm BG, Bradley WE. Cortical evoked responses from the perineal nerve. J Urol 1999;162: [7] Yang CC, Bradley WE. Reflex innervation of the bulbocavernosus muscle. BJU Int 2000;85: [8] Yucel S, Baskin LS. Neuroanatomy of the male urethra and perineum. BJU Int 2003;92: [9] Barbagli G. Words of wisdom. Re: neuroanatomy of the male urethra and perineum. Eur Urol 2006;50:1367. [10] Elthahawy EA, Virasoro R, Jordan GH. Vessel sparing excision and primary anastomosis of the urethra. J Urol 2006;175:104 (abstract no. 315). [11] Barbagli G, De Angelis M, Palminteri E, Lazzeri M. Failed hypospadias repair presenting in adults. Eur Urol 2006;49: [12] Manzoni G. Hypospadias repair failures: lesson learned. Eur Urol 2006;49: [13] Mundy AR. Failed hypospadias repair presenting in adults. Eur Urol 2006;49: [14] Bracka A. Editorial Comment on: Failed hypospadias repair presenting in adults. Eur Urol 2006;49: [15] McKillop C. Interview with Dr Guido Barbagli. Substitution urethroplasty: which tissues and techniques are optimal for urethral replacement? Eur Urol 2007;52: [16] Barbagli G. Adherence to the right diagnostic tools for best outcomes in urethral reconstructive surgery. Eur Urol 2006;50:424 5.