Single-stage repair of obliterated anterior urethral strictures using buccal mucosa graft and dorsal penile skin flap

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1 International Journal of Urology (2019) 26, doi: /iju Original Article: Clinical Investigation Single-stage repair of obliterated anterior urethral strictures using buccal mucosa graft and dorsal penile skin flap Vladimir Kojovic, 1 Miroslav L Djordjevic 1 and Aleksandar Vuksanovic 2 1 Medical School, University of Belgrade, and 2 Clinic of Urology, Clinical Center of Serbia, Belgrade, Serbia Correspondence: Aleksandar Vuksanovic M.D., Ph.D., Clinic of Urology, Clinical Center of Serbia, Resavska 51, Belgrade 11000, Serbia. avuksano@mts.rs Received 11 April 2018; accepted 30 August Online publication 7 October 2018 Objective: To present a single-stage repair of obliterative urethral strictures by simultaneous use of a buccal mucosa graft and longitudinal dorsal penile skin flap. Methods: Between February 2007 and October 2016, 51 patients with obliterative anterior urethral stricture underwent single-stage substitution urethroplasty. A buccal mucosa graft was harvested and fixed to the corpora cavernosa as the dorsal part of the neourethra, and a vascularized dorsal penile skin flap was created, transposed ventrally and sutured to the buccal mucosa graft to form ventral part of the neourethra. Results: The follow-up period was months (mean 49 months). The mean age of the patients was 48 years (range years). The mean length of the obliterated urethral segment, measured during the operative procedure, was 5.2 cm. The etiology of strictures was: unknown, hypospadias and trauma in 19, 27 and five patients, respectively. Five patients were lost to follow up, and 46 patients were analyzed for the outcome. At the end of the follow-up period, recurrence of the stricture occurred in seven (15.2%) patients, whereas 39 (84.8%) patients did not develop stricture. An additional three (6.5%) patients developed fistula, resulting in overall successful voiding in 36 (78.3%) patients. Conclusions: A combined buccal mucosa graft and longitudinal dorsal penile skin flap could be a good choice for one-stage substitution urethroplasty in complex obliterative urethral strictures, with an acceptable complication rate. Key words: buccal mucosa graft, complex stricture, obliterative stricture, penile skin flap, urethral stricture. Introduction Repair of anterior urethral strictures usually includes augmentation urethroplasty in order to create a sufficient urethral lumen. Various skin flaps or a buccal mucosa graft can be sutured to the urethral mucosa to enlarge the narrow urethral channel. However, in patients with the most severe urethral strictures, urethral mucosa and corpus spongiosum could be heavily affected, and complete obliteration of urethral lumen might develop. The majority of these patients have already undergone a failed repair of hypospadias or severe urethral strictures. Patients with these obliterative strictures do not have salvageable urethral mucosa in the affected segment that can be used for restoration and, therefore, complete reconstruction of the whole urethral circumference is required. Standard treatment options in these cases include substitution with tubularized flaps or a staged repair with free grafts. Tubularized flap has been shown to lead to mostly unsatisfactory results with a significant failure rate. 1,2 Staged repair with buccal mucosa has better outcomes, but a two-staged procedure is necessary. 3 Unfortunately, two-staged procedures easily become desperate multistaged procedures. 4 Our hypothesis was that severe obliterative strictures can be successfully cured in one stage, using both a buccal mucosa graft and penile skin flap. Therefore, the purpose of this study was to present outcomes of the one-stage reconstruction of obliterative anterior urethral strictures using a combination of a buccal mucosa graft and longitudinal dorsal penile skin flap The Japanese Urological Association

2 Repair of obliterated urethral stricture Methods Between February 2007 and October 2016, a total of 51 patients with obliterative anterior urethral stricture underwent single-stage substitution urethroplasty. All patients enrolled in the study had a complex stricture that included variable length of the urethral segment without salvageable urethral mucosa. A new urethral lumen was created using both a buccal mucosa graft and longitudinal dorsal penile skin flap in all patients. Patients with clinical signs of lichen sclerosus and/or severely scarred penile skin were not eligible for this procedure. The preoperative studies included urethroscopy, when feasible, with a 9-Fr pediatric cystoscope, retrograde urethrography and descendent urethrography. Some patients underwent preoperative ultrasonography to verify the extent and the length of spongiofibrosis. The study was approved by the institutional ethics committee, and informed consent was obtained for all patients. Surgical procedure The patients were positioned in the supine position for strictures in the distal penile part of the urethra; or in the lithotomy position for repairs in the bulbar urethral segment. A standard circumferential subcoronal incision was made, followed with penile skin degloving. The affected urethral segment was completely removed, as it was severely scarred with no viable urethral mucosa (Fig. 1). All tissue with spongiofibrosis was excised proximally until healthy urethral tissue with a normal urethral caliber was reached. A buccal mucosa graft of an appropriate size was harvested from the inner cheek using a standardized technique, and the donor site was closed with a running suture. The length of the graft exceeded the size of the missing urethral segment by approximately 10%, for a fully stretched penis; whereas the width was approximately 15 mm. Excessive fat tissue was trimmed from the graft, and it was thoroughly quilted to the corpora cavernosa, and sutured to the distal and proximal urethral mucosal segment. In this manner, the neourethral plate; that is, the dorsal half of the neourethra, was created. A vascularized fasciocutaneous flap was created in longitudinal orientation using dorsal penile and preputial skin (Fig. 2). The approximate width of the skin flap was mm. The flap was transposed ventrally by a button-hole maneuver (Fig. 3). A running suture was used to join the skin flap (ventral half of the neourethra) to the lateral edges of the buccal mucosa graft over the 16-Fr silicone catheter (Fig. 4). The skin flap was anastomosed to the proximal and distal urethral segment in an oval shape. This way, a complete urethral lumen was created. An abundant pedicle of the fasciocutaneous flap was fixed laterally to cover all suture lines of the neourethra (Fig. 5). At the end of the procedure, covering of the penile shaft was carried out using available penile skin (Fig. 6). A compressive dressing was applied on the penis in a stretched position and a suprapubic urinary catheter was inserted. The transurethral catheter was removed 3 weeks after the procedure, whereas the suprapubic catheter was usually removed 5 7 days later. Standard broad-spectrum antibiotic prophylaxis was used while catheters were present. Patients Fig. 1 Obliterative anterior urethral stricture after failed hypospadias repair. No viable urethral mucosa can be used for urethral reconstruction. were advised to use a penile traction device or vacuum pump starting 4 weeks after the surgical procedure for a period of 3 months to avoid graft retraction and occurrence of penile curvature. Results The postoperative follow-up period ranged from 12 to 129 months (mean 49 months). The mean age of the patients was 48 years, and ranged from 15 to 71 years. The mean (SD) length of the obliterated urethral segment, measured during the operative procedure, was 5.2 cm (3.9 cm). The stricture was localized in the penile part of the urethra in 38 patients. The penile and bulbar part were affected in seven patients, and six patients had a structure limited to the bulbar urethra. The etiology of strictures was: unknown, hypospadias and trauma in 19, 27 and five patients, respectively. A total of 39 (76%) of all patients already underwent failed urethral repair before our procedure. Patients underwent retrograde urethrography 3 weeks after the surgery, before removal of the catheter, and uroflowmetry and ultrasonography to assess post-void residual urine volume. Urethroscopy was carried out if a patient reported difficulties with voiding (hesitancy, 2018 The Japanese Urological Association 91

3 V KOJOVIC ET AL. Fig. 2 Harvesting of a vascularized longitudinal dorsal penile skin flap. A button-hole is created at the base of the flap. straining, weak urine stream, dribbling) or recorded a maximum urinary flow rate <15 ml/s. The outcome was considered successful if the patient reported normal voiding, without the need for any additional surgical procedure open or endoscopic including urethral dilatation. Failure was defined as a maximum flow rate <15 ml/s, or voiding difficulties with stricture confirmed by a retrograde urethrogram or urethroscopy that required endoscopic intervention, dilatation or urethroplasty. The Kaplan Meier method was used to evaluate the success rate of stricture-free survival, and the v 2 -test was used to assess whether the length of the stricture influenced surgical outcomes. Five patients were lost to follow up, and 46 patients were analyzed for the outcome. Twelve months after surgery, 42 (91.3%) patients were stricture-free, and 24 months after surgery, 40 (86.9%) patients were stricture-free (Fig. 7). Eventually, recurrence of the stricture occurred in seven (15.2%) patients, whereas 39 (84.8%) patients did not develop a stricture during the follow-up period (grade IIIb Clavien Fig. 3 A buccal mucosa graft is harvested and fixed to the corporal bodies to create a new urethral plate. The skin flap is transposed ventrally by a button-hole maneuver. Classification of Surgical Complications). 5 Six patients with recurrence initially had a stricture in the penile part of the urethra, and one had a bulbar urethral stricture. Three (6.5%) patients developed a urethrocutaneous fistula, and all of them had a penile urethral stricture. Overall, successful voiding was achieved in 36 (78.3%) patients. Patients with longer strictures were likely to develop recurrence: six patients with recurrence of the urethral stricture had a urethral stricture >4 cm in length, whereas only one had a stricture <4 cm in length (v 2 = 4.337; P = 0.037). Five of the restenosis were located at the site of proximal anastomosis, and two in the distal anastomosis between the neourethra and the native urethra. These recurrent urethral strictures required additional repair: four of them were solved in one redo procedure and two in multistage repairs, whereas one patient with restricture of the bulbar urethra was repaired by internal urethrotomy. Two out of three patients with fistulas required surgical closure (grade IIIa Clavien), whereas one fistula resolved The Japanese Urological Association

4 Repair of obliterated urethral stricture Fig. 4 The complete urethral lumen is restored by joining the skin flap to the buccal mucosa graft. Fig. 5 After the urethral reconstruction, the abundant and wide pedicle of the skin flap completely covers suture lines of the neourethra. spontaneously during the follow-up period (grade I Clavien). Minor superficial necrosis of the dorsal penile skin (grade II Clavien) developed in five (10.9%) patients, and all healed by conservative treatment. Three (6.5%) patients reported altered sensation over the penile skin, and two (4.3%) patients reported post-voiding dribbling (grade I Clavien). Complications of the procedure are listed in Table 1. There were no significant complications related to the buccal mucosa harvest site. Patients reported pain and temporary numbness of the cheek (grade I Clavien Classification) in 22 (47.8%) and 10 (21.7%) patients, respectively. Discussion All attributes of every urethral stricture should be precisely defined to obtain an adequate approach and, subsequently, to achieve a successful outcome. Penile and bulbar urethral strictures with salvageable urethral mucosa and relatively healthy spongy tissue could be successfully repaired using either a buccal mucosa graft or penile skin flap, whereas complex non-obliterative urethral strictures often required a staged approach. 6 9 In our center, patients with anterior urethral strictures, where a viable strip of urethral mucosa can be found, are usually repaired by standardized buccal mucosa graft augmentation urethroplasty. 10,11 In contrast, the approach is much more questionable in patients with complex obliterative urethral strictures. The obliterative strictures are completely obstructive urethral strictures with a total loss of viable urethral mucosa in the affected segment. They are usually followed by severe spongiofibrosis. Complete reconstruction of the whole urethral circumference is required in these patients. Excision of the obliterated segment and primary urethral anastomosis ( endto-end ) presents optimal treatment only for short strictures located in the bulbar urethra. Anastomotic repair in penile urethra is not recommended because of a higher failure rate and subsequent penile curvature. A circumferential urethral segment needs to be created if complete obliteration of the anterior urethra is found. Single-stage repair of these strictures is debatable because of the unacceptable failure rate if a tube flap or graft is used. 1,2,6 Therefore, the majority of urologists opt for a two-stage approach for these severe cases, which was initially described by Johanson, and afterward modified by Bracka. 3,12 The obliterated urethral segment is replaced by a neourethral plate made of a buccal mucosa graft, which is tubularized 3 6 months later. Despite the higher success rate, this approach often leads to patients dissatisfaction because of the delay in treatment and the fact that two-stage procedures can easily become multistage procedures. 4,13 15 Different centers reported that 18 39% patients require revision of first-stage buccal mucosa urethroplasty, mainly due to severe contracture of the graft Furthermore, a significant number of patients who undergo first-stage urethroplasty never opt for second stage, possibly because they resolved the obstructed and painful voiding, as well as urinary tract infections, while avoiding the future risk of another surgery The Japanese Urological Association 93

5 V KOJOVIC ET AL. Table 1 Complications of the surgical procedure Complication Clavien grade 5 No. patients (%) Hematoma I 4 (8.7) Altered skin sensation I 3 (6.5) Post-void dribbling I 2 (4.3) Fistula (healed spontaneously) I 2 (4.3) Superficial skin necrosis II 5 (10.9) Fistula (surgery required) IIIa 1 (2.2) Recurrent stricture IIIb 7 (15.2) Fig. 6 Sucess rate Rearranging of the available skin to cover the penile shaft Follow-up (months) Fig. 7 Success rates of stricture-free survival in patients undergoing a combined buccal mucosa graft and penile skin flap urethroplasty for obliterative urethral strictures. Complete replacement of the urethral circumference by simultaneous use of a buccal mucosa graft and skin flap was initially described by Morey. 16 Erickson et al. reported a high success rate (78%) in their series of patients where this approach was used for circular urethral deficiency. 17 These authors presented favorable outcomes of combined tissue transfer in comparison with flap tubularization. If the combined approach is used, the healing of the dorsal and ventral aspect of neourethra relies on two distinct blood sources, which ultimately lead to better survival and, second, thorough fixation improves the stability of the neourethra with less possibility for retraction and recurrence. 17 Gelman and Sohn reported favorable outcomes in their series of patients treated by a similar approach. 18 Berglund and Angermeier proved that the combination of a buccal mucosa graft and penile or scrotal skin flap is a reliable and durable method of single-stage repair for extensive urethral stricture disease. 19 Several authors reported simultaneous use of two buccal mucosa grafts for circumferential urethral replacement Similarly, Chen et al. and Palminteri et al. presented their approaches where the combination of a buccal mucosa graft and full thickness skin graft was used in the repair of long and complex urethral strictures. 24,25 Undoubtedly, the combination of two grafts can increase the success rate in severe strictures, but this approach can be applied in patients with a healthy underlying bed for graft intake. Unfortunately, the majority of patients with obliterative urethral stricture, in particular after hypospadias repair, have excessive scarring and no viable spongiosal tissue. Alternatively, the tunica vaginalis flap can be used for additional support of a buccal mucosa graft placed ventrally. 23 However, a skin flap with its own blood supply presents the versatile option for reconstruction of the ventral aspect of the neourethra in these complex cases. We have favored the dorsal longitudinal skin flap over the transversal or circumferential flap because, in our experience, the risk of complications appears to be less. The creation of a longitudinal island skin flap has been previously reported in detail. 26 The majority of patients with circumferential urethral deficiency underwent failed hypospadias repair. The dorsal penile skin in hypospadias patients is almost always superior in abundance and vascularity in comparison with the ventral skin. Furthermore, the longitudinal orientation of the flap follows the axial course of blood vessels. The axial course of the blood vessels enables the creation of a wide hole for transposition of the flap using a button-hole maneuver with previous transillumination to prevent damage of the blood vessels. This flap is up to 15 mm wide, because there is no need for tubularization. After suturing the longitudinal skin flap and buccal mucosa graft, subcutaneous tissue of the flap can be easily fixed to corporal bodies around the new urethra. In this way, abundant subcutaneous tissue covers all suture lines, thus preventing fistula formation. Two remaining lateral skin flaps are usually wide enough to cover the penile body shaft thereafter. Finally, we believe that penile rotation, as a complication, is less likely to occur if the longitudinal orientation of the flap is used and if the flap is transposed ventrally by a button-hole maneuver. Pediatric patients with severe hypospadias, as well as transgender patients, are treated in our center using the same principle for urethral substitution. We realized that the present method of urethral substitution is reproducible and it could be easily applied in all patients suffering from urethral deficiency, not only for patients with obliterative urethral stricture. Scarce and short urethral plate in complex hypospadias cases cannot be used for urethral reconstruction, and new tissue must be found as a urethral substitute. The approach for creating the neourethra using the combination of a buccal mucosae graft and longitudinal penile skin flap proved its The Japanese Urological Association

6 Repair of obliterated urethral stricture effectiveness. 27 Furthermore, the creation of the neourethra in female-to-male transsexuals presents one of the most difficult segments of sex reassignment surgery. Again, the simultaneous use of a buccal mucosa graft and genital (clitoral or labial) skin flap was the best option for neourethral reconstruction in this complex group of patients. 28 In our opinion, the overall success of the simultaneous use of a buccal mucosa graft and penile skin flap is based on its independent reliable blood supply. Therefore, the described principle has shown favorable outcomes in the presented series, with an acceptable failure rate. Similar to the other authors, we have found that patients with longer strictures are more likely to develop strictures recurrence. Palminteri et al. reported that stricture length had been an independent risk factor for failure: the risk of having a reintervention was increased by 70% per cm of urethral stricture length. Strictures >4 cm in length presented a higher risk of failure compared with strictures <4 cm in length. 29 Breyer et al. also reported stricture length >4 cm to be an independent risk factor for failure. 30 Limitations of the present study were its retrospective design and the lack of a comparative group of patients with obliterative urethral strictures where a multistage approach was applied. Five patients in our series developed superficial necrosis of the dorsal penile skin. Disadvantage of presented surgical approach could be a paucity of available penile skin for relaxed covering of the penile shaft. Precise tailoring, harvesting and careful handling of the penile skin flaps are important steps for a successful outcome. Penile skin should not be used as a substitute for the urethra in patients with clinical signs of lichen sclerosus and severely scarred skin. The present study proved that the complete loss of urethral circumference can be successfully restored by the simultaneous use of a buccal mucosa graft and longitudinal penile skin flap. The main advantage of this approach is the possibility for effective one-stage repair, with a fairly acceptable complication rate. However, staged repair using a buccal mucosa graft remains the method of choice for patients with obliterative urethral strictures and clinical signs of lichen sclerosus or severely scarred penile skin. Acknowledgment This study was supported by the Ministry of Science, Republic of Serbia, with project No Conflict of interest None declared. References 1 McAninch JW, Morey AF. Penile circular fasciocutaneous skin flap in 1- stage reconstruction of complex anterior urethral strictures. J. Urol. 1998; 159: Wiender JS, Sutherland RW, Roth DR et al. Comparison of onlay and tubularized island flaps of inner preputial skin for the repair of proximal hypospadias. J. Urol. 1997; 158(Pt 2): Bracka A. A versatile two-stage hypospadias repair. Br. J. Plast. Surg. 1995; 48: Andrich DE, Greenwell TJ, Mundy AR. The problems of penile urethroplasty with particular reference to 2-stage reconstructions. J. Urol. 2003; 170: Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann. Surg. 2004; 240: Chapple C, Andrich D, Atala A et al. SIU/ICUD consultation on urethral strictures: the management of anterior urethral stricture disease using substitution urethroplasty. Urology 2014; 83(3 Suppl): S Barbagli G, Selli C, di Cello V et al. A one-stage dorsal free-graft urethroplasty for bulbar urethral strictures. Br. J. Urol. 1996; 78: Joshi PM, Barbagli G, Batra V et al. A novel composite two-stage urethroplasty for complex penile strictures: a multicenter experience Indian. J. Urol. 2017; 33: Mundy AR, Andrich DE. Urethral strictures. 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