Evaluate the use of lingual mucosal graft (LMG) in anterior urethral strictures.
From January 2001 to December 2006, 29 men (mean age, 48.5 yr) with anterior urethral strictures underwent graft urethroplasty with LMG. The mean length of stricture was 3.6 cm. Patients with bulbar, penile, or bulbopenile strictures received one-stage dorsal free graft urethroplasties. In patients with failed hypospadias repair we performed a two-stage urethroplasty. Criteria for successful reconstruction were spontaneous voiding with no postvoid residual urine and no postoperative instrumentation of any kind. Clinical assessment included the donor site morbidity.
Mean follow-up was 17.7 mo. One-stage bulbar and penile urethroplasties without meatal involvement had an 81.8–100% success rate. Bulbopenile urethroplasties were successful in 60% of the cases, whereas one-stage urethral reconstructions in patients with meatal involvement were successful in 66.6%. The two cases of two-stage urethral reconstruction with LMG and buccal mucosal graft after failed multiple hypospadias repairs were unsuccessful. The overall early recurrence rate was 20.7%. Patients with the graft harvested from the tongue reported only slight oral discomfort at the donor site and difficulty in talking for 1 or 2 d.
The mucosa of the tongue, which is identical to the mucosa of the rest of the oral cavity, is a safe and effective graft material in the armamentarium for urethral reconstruction with potential minor risks of donor site complications. LMG may be used alone for short strictures (<5 cm) or in combination with buccal mucosa when longer grafts are needed.
Keywords: Buccal mucosa, Free grafts, Hypospadias, Oral mucosa, Tongue, Transplants, Urethra, Urethral stricture, Urethroplasty.
Current opinion is that if free extragenital tissue is needed to perform urethroplasty, an oral mucosal graft provides excellent clinical results , , , , , and . In February 2006, we described the results of a pilot study on the use of the tongue as an alternative donor site for graft urethroplasty with good functional and aesthetic results . We now report our early experience with lingual mucosal grafts (LMGs) for urethral reconstruction in men with anterior urethral strictures.
From January 2001 to December 2006, 29 men, aged 20–77 yr (mean: 48.5 yr) with anterior urethral strictures underwent graft urethroplasty with LMG (unilateral or bilateral) or a combination of LMG (unilateral or bilateral) plus buccal mucosal graft (BMG; from the inner cheek).
The aetiology was iatrogenic (multiple hypospadias repair or free graft urethroplasty failures) in nine patients (31%), inflammatory in seven (24.2%), posttraumatic in five (17.2%), lichen sclerosus in seven (24.2%), and unknown in one (3.4%).
The stricture involved the penile urethra and meatus in 5 (17.2%), penile urethra in 8 (27.6%), bulbar urethra in 11 (37.9%), and the bulbopenile urethra in 5 patients (17.2%).
The mean length of stricture as measured intraoperatively was 3.6 cm (range: 1.5–9.8 cm).
All patients had undergone a number of previous treatments including dilation, optical internal urethrotomy, and urethroplasty.
All patients were evaluated preoperatively with uroflowmetry, flexible urethroscopy, and retrograde or voiding urethrography.
2.2. Surgical techniques
2.2.1. LMG harvesting technique
The LMG harvesting technique has been previously described in our pilot study .
However, we here illustrate step by step the technique that was refined during the past 6 yr. (1) A mouth opener may be placed but it is not mandatory. (2) The apex of the tongue is passed through with a 1-0 suture for traction or direct traction is applied with a Babcock clamp to expose the ventrolateral surface of the tongue (Fig. 1a). (3) The site of the harvest graft is the ventrolateral mucosal surface of the tongue, below the lining that separates the dorsum, where the papillae are situated, from the sublingual mucosa. (4) The required graft (which is not infiltrated with any solution) is measured and marked with a surgical pen after identification of the opening of the Warton duct (Fig. 1b). (5) The graft edges are incised with a scalpel and a full-thickness mucosal graft is harvested using sharp instruments beginning at the anterior land mark of the graft (Fig. 1c). A 4-0 traction stitch may be useful to better handle the graft. (6) The donor site is carefully examined for bleeding and easily closed with interrupted polyglactin 3-0 sutures (Fig. 1d). (7) When submucosal tissue is present, graft defatting is performed. When a further graft is needed the procedure may be performed on the contralateral side.
(a) The apex of the tongue is placed under traction to expose the site of the harvest graft, which is the ventrolateral surface of the tongue. (b) The required graft is marked with a surgical pen and the graft edges are incised with a scalpel. (c) A full-thickness mucosal graft is harvested using scissors. (d) The donor site is carefully examined for bleeding and easily closed with interrupted polyglactin 3-0 sutures. Blue drawing pin indicates the ranine vein. Orange arrow indicates the opening of Wharton's duct.
2.2.2. BMG harvesting technique
We used a standard BMG harvesting technique .
We used three different urethroplasty techniques (Table 1).
|Stricture aetiology||Stricture length, cm||Graft||Outcome|
|One-stage dorsal free graft urethroplasty|
|Penile strictures, n = 8|
|4||Lichen sclerosus||8.5||Bilateral LMG||Success|
|5||Lichen sclerosus||5.0||Unilateral LMG||Success|
|6||Lichen sclerosus||4.0||Unilateral LMG||Success|
|7||Lichen sclerosus||5.0||Unilateral LMG||Success|
|Total success rate 100%|
|Bulbar strictures, n = 11|
|4||Lichen sclerosus||3.0||Unilateral LMG||Success|
|10||Iatrogenic (free graft urethroplasty failure)||3.0||Unilateral LMG||Success|
|11||Iatrogenic (free graft urethroplasty failure)||1.5||Unilateral LMG||Success|
|Total success rate 81.8%|
|Bulbopenile strictures, n = 5|
|2||Lichen sclerosus||1.5||Unilateral LMG||Failure|
|3||Lichen sclerosus||4.0||Unilateral LMG||Failure|
|4||Iatrogenic (free graft urethroplasty failure)||1.5||Unilateral LMG||Success|
|5||Iatrogenic (hypospadia repair failure)||1.5||Unilateral LMG||Success|
|Total success rate 60%|
|Penile and meatus, n = 3|
|1||Iatrogenic (hypospadia repair failure)||5.0||Unilateral LMG||Failure|
|2||Iatrogenic (hypospadia repair failure)||2.0||Unilateral LMG||Success|
|3||Iatrogenic (hypospadia repair failure)||3.5||Unilateral LMG||Success|
|Total success rate 66.6%|
|Penile and meatus, n = 2|
|1||Iatrogenic (hypospadia repair failure)||9.0||Bilateral LMG + unilateral BMG||Failure|
|2||Iatrogenic (hypospadia repair failure)||7.0||Unilateral LMG + unilateral BMG||Failure|
|Total success rate 0%|
LMG = lingual mucosal graft; BMG = buccal mucosal graft.
Patients with penile and meatal strictures underwent a one-stage dorsal free graft urethroplasty with a ventral sagittal urethrotomy approach . Briefly, a subcoronal incision is made, the penis is degloved, and the urethra is exposed. A ventral incision is made to open the strictured urethra. The dorsal urethral plate is longitudinally incised up to the corpora cavernosa and the glans. The wings of the urethral plate are laterally mobilised to create the bed for the graft. The graft is sutured and quilted on the bed of the dorsal incision with polyglactin 5-0 sutures with the result of an augmented plate. The urethra is closed and tubularised over a 14-Ch catheter. The glans and the penile skin are closed over the urethra.
In patients with failed hypospadias repair we performed a two-stage urethroplasty . In the first stage the urethral plate was removed and the oral mucosa graft was splayed and quilted over the tunica albuginea. After 6 mo the urethra was tubularised over a 14-Ch catheter.
Postoperatively all patients were followed with pericatheter urethrography and voiding cystography after 2 wk and uroflowmetry, cystourethrography, and flexible urethroscopy after 3 and 12 mo. The criteria for successful reconstruction were spontaneous voiding with no postvoid residual urine and no postoperative instrumentation of any kind. The clinical assessment included the donor site morbidity with evaluation of presence of oral pain, difficulty of mouth opening or talking, neurosensory deficits, and salivary changes.
3.1. Urethroplasty outcome
Mean follow-up was 17.7 mo (median: 21 mo; range: 6–71 mo).
Pericatheter urethrography performed after 2 wk showed two cases of periurethral leakage, which healed spontaneously with prolonged catheter drainage for another week.
In 23 (79.3%) of the 29 cases, surgery was successful; in 6 (20.7%) surgery was considered a failure at the 3 mo follow-up evaluation. All six restrictures developed within 3 mo from surgery and were treated with coaxial dilation up to 20 Ch with improvement of the symptoms and a peak flow rate of 9.3 ml/s (range: 6–12 ml/s). No other major perioperative complications occurred. Table 1 summarises the outcome related to the stricture location, stricture aetiology, and surgical technique.
One-stage bulbar and penile urethroplasties without meatal involvement had an 81.8–100% success rate.
Bulbopenile urethroplasties were successful in 60% of the cases (in the two failures aetiology was lichen sclerosus), whereas one-stage urethral reconstructions in patients with meatal involvement were successful in 66.6% of the cases.
The two-stage urethral reconstruction with LMG and BMG in two men after failed multiple (6 and 13 different operations, respectively) hypospadias repairs was unsuccessful. However, in patients with penile and meatal urethral strictures the peak flow rate improved from a mean of 6.5 ml/s (range: 4.9–10.3 ml/s) to 10.4 ml/s (range: 7.9–16 ml/s). In patients with penile urethral strictures the peak flow rate improved from a mean of 4.3 ml/s (range: 0–8.5 ml/s) to 26.4 ml/s (range: 16–31 ml/s). In patients with bulbar urethral strictures the peak flow rate improved from a mean of 5.9 ml/s (range: 0–8.9 ml/s) to 31.2 ml/s (range: 9.2–64 ml/s). In patients with bulbopenile urethral strictures the peak flow rate improved from a mean of 7.6 ml/s (range: 3.2–13 ml/s) to 17.2 ml/s (range: 10.4–24.5 ml/s).
In all the successful cases cystourethrography and flexible urethroscopy revealed no significant graft contractures or sacculations. In the two patients with a two-stage urethroplasty and an unsuccessful functional result, LMG was nearly indistinguishable from BMG after the first stage, revealing equivalent imbibition, inosculation, and revascularisation properties (Fig. 3).
3.2. Donor site evaluation
The length of LMG used ranged from 3 to 9 cm (mean: 5.3 cm); the LMG width was always about 1.5 cm.
The graft was harvested unilaterally from the tongue only in 25 patients (86.2%), bilaterally from the tongue only in 2 (6.9%), unilaterally from the tongue plus unilaterally from the inner cheek in 1 (3.5%), and bilaterally from the tongue plus unilaterally from the inner cheek in 1 (3.5%).
All patients reported just slight oral discomfort within the first 3 d postoperatively. All patients were able to assume oral fluids within 24 h, eat soft solids in 48 h, and return to a normal diet after 1 wk. Fig. 2 illustrates the lingual donor site at 0, 15 d, 6 mo, and 12 mo.
(a) Intraoperative aspect of the donor site, (b) after 15 d, (c) after 6 mo, and (d) after 12 mo.
Difficulty of mouth opening was present for about 36 h in the patients who had the graft harvested from the inner cheek.
Oedema of the tongue with a slight difficulty in talking was present for about 24 h when a unilateral graft was harvested and for about 48 h when a bilateral graft was harvested.
In the single case with the graft harvested bilaterally from the tongue and unilaterally from the inner cheek, reduced salivatory flow was present for about 3 mo.
A neurosensory deficit of the donor site resolved in about 2 mo in the two patients with the graft harvested from the inner cheek.
Urethroplasty techniques continue to improve but there is no definitive answer regarding the superiority of one approach over another.
A large variety of free extragenital graft tissues has been used for urethroplasty, such as the ureter, saphenous vein, appendix, full-thickness skin, bladder, and colonic or buccal mucosa  and . Recently, collagen matrices, such as the porcine small intestinal submucosa, have been used for urethroplasty showing potential good results; their efficacy is currently under evaluation  and .
Today, if free extragenital tissue is needed to perform urethroplasty, an oral mucosal graft is considered the best tissue providing excellent clinical results , , , , , and . The use of oral mucosal grafts prevents the cosmetic disadvantages caused by use of local genital skin such as penile/glans torsion, subcutaneous deformities, and chordee.
So far, the oral mucosal grafts were harvested from the mucosa of the inner cheek or from the mucosa of the lip .
4.1. The LMG for urethral reconstruction
We recently demonstrated the feasibility of LMG use for urethral reconstructive surgery . The ventrolateral aspect of the tongue offers mucosal tracts that are up to 7–8 cm long, depending on the tongue dimensions, and has constant availability. Like buccal mucosa, the lingual mucosa has the same embryologic origin, easy harvesting, favourable immunologic properties (resistance to infection) and tissue characteristics (thick epithelium, high content of elastic fibers, thin lamina propria, rich vascularisation) that are favourable properties for imbibition, inosculation, and revascularisation of the graft .
The similar favourable revascularisation properties are evident when the BMG and LMG are simultaneously used during a two-stage urethroplasty (Fig. 3).
Six mo after implant the BMG and LMG grafts are indistinguishable.
When compared with the published results of BMG, our early results with the use of LMG appear similar.
In our experience, one-stage bulbar and penile urethroplasties without meatal involvement had an 81.8–100% success rate, the same rates obtained with BMG . Patients in our series showed a 20.7% overall early recurrence rate.
Bulbopenile urethroplasties were successful in 60% of the cases and one-stage urethral reconstructions in patients with meatal involvement were successful in 66.6% of the cases. Two-stage urethral reconstruction after several unsuccessful hypospadias repairs failed in two patients. However, it is well known that urethral reconstructions after failed hypospadias repairs are prone to worst results and complications . Additional follow-up is required to evaluate the patients with lichen sclerosus for the risk of long-term failure .
The tongue offers mucosal tracts that are up to 5–8 cm long but in the majority of patients it is possible to obtain grafts of about 5 cm length. Therefore, an LMG may be safely used for strictures that are <5 cm long.
An advantage of having the tongue in the armamentarium of grafts is its possible integration in patients with extremely long strictures when a long graft is needed and the BMG is not sufficient. In this way it is possible to avoid the use of lower lip mucosa, which is prone to oral complications and extragenital or heterologous grafts.
4.2. Donor site complications
BMG harvesting is an excellent procedure, but it carries long-term oral complications, although they are infrequent.
The main long-term donor site complications are persistent perioral numbness, salivatory changes, and difficulty in opening the mouth  and . Other complications are bleeding , scarring, and lip deviation or retraction  and .
The lateral aspect of the lingual mucosa has no particular functional features and almost half of the tongue tissue can be used as donor tissue, as in cancer of the tongue, without imposing any functional limitations on it . We never observed major intraoral complications, such as persistent numbness, salivatory changes, difficulties with mouth opening, deviations, or retractions. Patients with the graft harvested from the tongue reported only slight oral discomfort at the donor site and difficulty in talking for 1 or 2 d. Transitory (<3 mo) difficulty of mouth opening, neurosensory deficit, and reduced salivatory flow were present in the two patients who had the graft harvested from the inner cheek.
Markiewicz et al , according to standard and accepted dental terminology, recommend the term “labial mucosa graft” when referring to the alveolar mucosa of the inner lower lip and the term “buccal mucosa graft” when referring to the alveolar mucosa of the inner cheek. Both terms should collectively be denoted as the “oral mucosa graft.” We agree with the authors. However, according to our experience and considering the embryologic origin and anatomic knowledge, we think that the term “oral mucosa graft” should include the LMG.
Therefore, to avoid confusion between the inner lower lip and the lingual grafts we would suggest a different terminology as follows.
The term “oral mucosa graft” (OMG as a standard acronym) should include three graft donor sites: the inner lower lip (LMG as a standard acronym), the inner check (BMG as a standard acronym), and the tongue (TMG as a new standard acronym). The bladder mucosa graft should be referred in a different way to avoid confusion (eg, “urinary bladder mucosa graft” with UBMG as a standard acronym).
Based on our experience, the mucosa of the tongue, which is identical to the mucosa of the rest of the oral cavity, is a safe and effective graft material in the armamentarium for urethral reconstruction with a minor risk of donor site complications. LMG may be used alone for short strictures (<5 cm) or in combination with BMG when longer grafts are needed. Future comparative studies will be necessary to compare the results with BMG. Our initial results are encouraging but additional work and a strict follow-up are necessary to compare critically the outcomes with other graft materials and to make final conclusions.
Conflicts of interest
The authors have nothing to disclose.
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a “Luciano Giuliani” Department of Urology, University of Genoa, Genoa, Italy
b Department of Urologic Surgery, “Luigi Sacco” University Medical Center, Milan, Italy
Corresponding author. Ospedale San Martino, Clinica Urologica “L. Giuliani”, pad. 12, Università degli Studi di Genova, L.go Rosanna Benzi, 12, 16132 Genova, Italy. Tel. +393356444088; Fax: +39010354004.
© 2008 European Association of Urology, Published by Elsevier B.V.