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Annals of African Medicine, Vol. 8, No. 4, October-December, 2009, pp. 203-209 Review Article Oral mucosa grafts for urethral reconstruction Mungadi IA, Ugboko VI Department of Surgery, Usmanu Danfodiyo University Teaching Hospital, Sokoto Code Number: am09045 PMID: 20139540 Abstract Background: Urethral reconstruction has continued to present formidable and enormous challenges for urologic, paediatric and plastic surgeons as diverse opinions have been expressed on the quality and type of ideal substitution material. This literature review is aimed at drawing attention of surgeons to the versatile nature of oral mucosal grafts.Methods: A review of the utilization of oral mucosa in urethral reconstruction was made. Structured Medline search was performed looking at all aspects of utilization of oral mucosa including mucosal harvest, donor site morbidity and outcome. Results: The unique demands of the urethra set a high standard for autogenous graft substitutes; hence literature reports reveal that split and full thickness skin grafts from the scrotum, penis, extragenital sites (ureter, saphenous vein, appendix, colon, medial upper arm, neck, lateral chest, abdomen, bladder mucosa) and more recently oral mucosa have been used. Unlike other tissues, oral mucosa grafts are flexible, easy to harvest and trim and have an excellent microvasculature favorable for graft-taking. Furthermore, the natural moist location of the oral mucosa in the oral environment favours its easy adaptability in the urethral passage thus giving good long-term results. However, there are reports of complications at the donor site with the commonest being anaesthesia or paraesthesia of the cheek or lips. Regional variations of the oral mucosa, length of the graft required, the decision to close or leave donor site open and harvesting technique are some of the factors suggested to account for differences in donor site morbidity. Conclusion: Oral mucosal graft is a versatile urethral substitute with excellent outcome. It is becoming the gold standard for urethral substitution. Keywords: Oral mucosa, graft, urethroplasty Introduction Worldwide and over the years, reconstruction of the urethra has continued to present formidable and enormous challenges for urologic, pediatric and plastic surgeons as diverse opinions have been expressed on the quality and type of ideal substitution material. The unique demands of the urethra set a high standard for autogenous graft substitutes. [1] Reports show that split and full-thickness skin grafts from the scrotum, penis and extragenital sites (ureter, saphenous vein, appendix, colonic mucosa, medial upper arm, neck, lateral chest and abdomen), bladder mucosa and, more recently, oral mucosa have been used. [2],[3],[4],[5],[6] Skin provides abundant material that is easy to harvest, but its keratinized epithelium and split-thickness depth increase susceptibility to postoperative contracture, stricture formation and graft thickening when tabularized. [6] The skin hair also constitutes a major problem when hairy skin is used as a graft for urethral reconstruction. Bladder mucosa is more difficult to harvest, especially in patients who have had previous bladder surgery, exstrophy, chronic cystitis or neurogenic dysfunction. Furthermore, increased morbidity, meatal prolapse, stenosis and ectropion formation have been associated with the use of bladder mucosa. [1] Unlike bladder mucosa and skin, buccal mucosa has a thick nonkeratinized epithelial layer and a well-vascularized and thin lamina propria, favoring early inosculation. [7] Buccal mucosal grafts have emerged as reliable substitutes with long-term results comparable to those of penile skin flaps. [8],[9] Some authors have recommended buccal mucosa over flaps for patch urethroplasty. [10],[11] Buccal mucosa takes shorter time to harvest compared with penile flaps and spares the penis from potential complications of scarring (donor site), torsion and cordee. The chances of failure and recurrence are reduced in patients with balanitis xerotica obliterans as buccal mucosa is not involved in this process. [12] Historical Perspective Oral mucosa has been used as a free graft in reconstructive plastic surgery for over a hundred years, since Stellwag von Carion used the lip mucosa to repair conjunctival defects in 1873. [3] As early as 1941, Humby combined oral mucosa with a full-thickness graft for penoscrotal fistula closure and observed success with only the buccal mucosa. [13] El-Kasaby et al., have described their experience with 20 patients undergoing 1-stage correction of an anterior urethral stricture using a buccal mucosa patch graft; they obtained excellent results in 18 patients. [14] Similarly, Monfort et al., managed strictures in pediatric patients and noted a comparable success rate of 90% for bladder mucosa and oral mucosa. [15] After these initial publications, 1994 onwards several clinical accounts have been published on the use of oral mucosa, especially for small populations of patients. [16],[17] The first large heterogeneous patient sample ( n = 18) was presented by Duchett et al., where after 27 months of follow-up, 17% of the patients required corrective surgery. [18] Their report also contained the first histological and immunohistochemical investigations of the oral mucosa compared with penile skin and bladder mucosa, and it is noteworthy that their findings explained the quick acceptance of this free graft. Dessanti et al., also reported their findings from 12 cases after the first long follow-up of 3 years with encouraging results. [19] Since 1995, buccal mucosa graft (BMG) has been used more often than penile skin for urethral reconstruction. [20] [Table - 1] summarizes the historical perspective of oral mucosa grafts for urethroplasty. The year 1996 saw the publication of the largest clinical series (100 cases), where after a follow-up of 23 months, only 12% had complications. [21] Subsequently, other publications focused on techniques of harvesting the graft, as well as the available sites that could avoid or minimize donor site morbidity. [1],[20],[21],[22],[23],[24],[25],[26],[27] This led Filipas et al., to attest to the long-term suitability of mucosal grafts after exposure to urine. [3] The period from the late 1990s to the present times has seen more articles focusing on donor site morbidity in cases of oral mucosal grafts and its implications. The higher prevalence of donor site complications seen in recent reports [5],[28],[29],[30],[31],[32] contrasts with the findings of earlier workers [1] probably due to greater attention on the complications following urethroplasty than on the potential complications associated with harvesting oral mucosal graft. There are also studies comparing postoperative morbidities at different intraoral sites, the latest site studied being the lateral surface of the tongue. [31],[32],[33] Surgical Anatomy of Oral Mucosa The morphology of oral mucosa varies from region to region being related to the functional demands placed upon it. These regional differences exist in the nature of the submucosa, the composition of the lamina propria, the morphology of the epithelial-connective tissue boundary, the thickness of the epithelium and type of keratinization. Three types of oral mucosae have been described, viz., masticatory, lining and specialized mucosae, and researchers have explored the use of mucosal grafts from the buccal and lower lip and from the lateral surface and undersurface of the tongue. Buccal and labial mucosae These are covered by lining mucosa and have a stratified squamous nonkeratinized epithelium that lines a thin elastic lamina propria and submucosa [Figure - 1]. The lamina propria consists of a rich vascular supply and dense connective tissue with short, irregular dermal papillae; while the submucosa is firmly attached to the underlying buccinator and orbicularis oris muscles and contains minor salivary glands [Figure - 2]. After the removal of its subcutaneous tissue, buccal mucosa is relatively thick, mechanically stiff and elastic and so easy to handle. It is also suggested to have an infection defense layer denoted by a high concentration of IgA antibodies as a result of evolution-related qualities. [3],[34] Furthermore, the natural moist location of the buccal mucosa in the oral environment favors its easy adaptability in the urethral passage when used as a free graft. [35],[36] The mucous membranes of the cheek and lower lip receive their nerve supply from the buccal and mental branches of the mandibular nerve, respectively. The lip mucosa is thinner and less resistant than the buccal mucosa. In addition, the width of the lip (maximal dimension, 1 x 4 cm), unlike the buccal mucosa (maximal dimension, 3 x 5.5 cm), limits the size of the graft. [1],[37],[38] Tongue mucosa The mucosa covering the lateral surface and undersurface of the tongue is identical in structure to that lining the rest of the oral cavity, hence it is constantly available with favorable immunological properties (resistance to infection) and tissue characteristics (thick epithelium, high content of elastic fibers, thin lamina propria and rich vascularization) and is also easy to harvest. [33] The lateral surface of the tongue offers a short mucosa, of about 7-8 cm long, and both lateral surfaces are available as donor sites if the need arises. [33] Indications/Uses of Oral Mucosal Free Grafts Oral mucosal free graft is indicated where urethral substitution is required as an alternative to skin. It may be applied for a dorsal, lateral or ventral onlay repair or for augmented anastomotic urethroplasty. Buccal mucosa has displaced genital skin flaps and grafts for onlay procedures in several centers. [20] Barbagli et al., championed dorsal placement of graft suggesting that dorsal placement gives better vascular and mechanical support, promoting take and reducing incidence of pseudo-diverticulation and enterenteneous fistula. [30] Several studies later supported this position. [20],[25],[39],[40] Other reports have shown no differences in outcome with respect to dorsal, lateral and ventral placements of graft. [41],[42] Oral mucosa may also be used in staged urethroplasty for complex urethral stricture [43],[44] and in revision urethroplasty for failed hypospadias repair. [45],[46] Staged buccal graft re-operation creates a well-vascularized substitute urethral plate for easy tubularization during the second stage. [47] Buccal mucosa is currently also employed in several reconstructive procedures, including glans recovering, vaginoplasty, ureteric reconstruction, metoidioplasty and repair of stenotic catheterizable continent stoma. [48],[49] Harvesting Techniques Oral mucosa can be harvested from the cheek or lower lip, as shown in [Figure - 3] and [Figure - 4]. Where a long length is needed, the inner cheek strip can be taken continuous with the lip. Typically the circumference of the adult urethra is between 22 and 24 mm, and a 6 cm length is often adequate for most strictures; hence some workers have described various techniques of harvesting oral mucosal graft. [1],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40],[41],[42],[43],[44],[45],[46],[47],[48],[49],[50],[51] Tolstunov and Pogrel described the free buccal mucosa graft procedure taken under general anesthesia using the Steinhauser mucosal stretcher with retractor (Walter Lorenz Surgical, Inc., Jacksonville, Fla). [23] This instrument served as a retractor, assisted in achieving hemostasis by the spring-acting squeezing action between the plates and defined the donor site (63 x 48 mm window) inside the intraoral plate. Submucosal local anesthesia was administered to decrease bleeding and define tissue planes. The graft was thereafter taken with a scalpel, and a tenotomy scissors was used to carefully dissect to the lamina propria separating the graft from the bucopharyngeal fascia. The donor site was subsequently closed with interrupted and continuous sutures. On an average, a graft of 6 x 2.5 cm was harvested. However, Tolstunov et al., have suggested outlining of the donor graft site before harvesting, making sure that at least an 8-mm distance is maintained away from the papilla of the parotid duct and 1 to 1.5 cm behind the commisure of the mouth to prevent distortion of the vermillion border during dissection. [51] They also advised that care should be taken when suturing the mucosa not to involve the duct lower lip wound is not closed to prevent inversion of the lip. Some authors have suggested that donor sites should be left open as this approach may reduce postoperative pain with no additional morbidity. [30] Eppley et al., opined that harvesting a graft from the buccal mucosa was more challenging due to limited access from the posterior location of the donor site. [1] The donor site was described as the area extending from the anterior tonsillar pillar to the vermillion-mucosal junction of the commisure, while the superior margin was a line some millimeters below the level of the parotid duct. Inferiorly it extended to the level of the mandibular vestibule, thereby providing a donor site of about 16.5 cm 2 (measuring 3 x 5.5 cm). They recommended nasoendotracheal intubation and improved access to the donor site by insertion of a Dingman intraoral retractor that permits maximal mouth opening, stretching and lengthening of the buccal mucosa. The procedure of graft-taking was quite similar to that described by Tolstunov and Pogrel except for separation of the mucosa using cautery and subsequent rinsing of the graft with antibiotic solution before placement in the recipient site. [23] Eppley et al., and Fabbroni et al., also closed the donor site partially, starting from the anterior edge, with absorbable sutures and making sure there was no bunching anteriorly. [1],[27] However, Fabbroni et al., observed that an elliptical incision would have allowed for primary closure of the donor site but this would have been at the expense of a smaller graft. Recently, Simonato et al., advocated and described a technique of harvesting mucosal graft from the lateral surface of the tongue. [33] Irrespective of the method of harvest and site, the harvested graft should be appropriately de-fattened and applied according to the indications. Donor Site Morbidity Most surgeons have focused more on the complications following urethroplasty than on the potential complications associated with harvesting buccal mucosal graft. As a matter of fact, earlier reports have indicated a low prevalence of morbidity and complications at the donor site following oral mucosa grafts for urethral reconstruction; but it was not until recently that other researchers started documenting their contrasting experiences. [1],[29],[30],[31],[32] Amongst the complications highlighted in the literature are intraoperative hemorrhage, postoperative infection, pain, swelling, damage to the parotid duct, limitation of mouth opening, eversion of the vermillion, loss of sensation or altered sensation in the cheek or lower lip as a result of damage to the long buccal or mental nerves and scar contracture. [1],[23],[29],[30],[31],[32] Transient paresthesia of the lower lip following neuropraxia of the mental nerve has been observed as the commonest complication. [5],[31] Up to 57% of the cases seen by Dublin and Stewart developed numbness after surgery. [28] Neurosensory deficit of the long buccal and mental nerves could be explained by individual variations in the location and type of branching of these two nerves; for injury could occur to the long buccal nerve if the incision extends too far posteriorly and inferiorly. Similarly the mental nerve could be damaged if the incision is extended too far anteriorly. This is particularly pertinent in short and thin individuals who have limited amount of buccal mucosal tissue. [51] Wood et al., reported the impact of donor site closure on morbidity, while Kamp et al., and Jang et al., compared donor site morbidities in both the lips and inner cheek and found significantly greater long-term complications after harvesting graft from the lower lip. [30],[31],[32] In addition, Greenwell et al., assessed the morbidity of buccal mucosa graft and the effect of non-suture of the graft site on postoperative pain. [52] They concluded that the donor site can be left unsutured to lessen pain. This contrasts with the findings of Dublin and Stewart, where all the donor sites were closed and about 32% of the patients had "tightness" of the mouth. [28] They also suggested secondary healing of the donor site to prevent the complication of lip eversion. Steinhauser had earlier observed that techniques involving full-thickness mucosal grafts leave a defect that must be closed by sutures, and this can cause scarring and contraction with decreased mouth opening. [50] Simonato et al., in a recent pilot study using mucosa of the lateral surface of the tongue reported no pain, esthetic or functional complications at the donor site, unlike the buccal mucosal graft. [33] However, the limited length of available mucosa on the lateral surface of the tongue makes it difficult to use in patients with long strictures. Regional variations of the oral mucosa, length of the graft required, the decision to close or leave donor site open and harvesting technique are some of the factors suggested to account for such differences. [31],[32] The Role of Tissue Engineering The main constraint of oral mucosa is the limited amount available for harvest in patients with extensive or panurethral strictures. Buccal mucosa has been successfully tissue-engineered by culturing oral keratinocytes and fibroblasts. These cells were applied to de-epidermised dermis to obtain full-thickness tissue-engineered oral mucosa for substitution urethroplasty. [53] Tissue-engineered mucosa may be utilized not only for urethral reconstruction but also for immediate reconstruction of intraoral tissue defects following oral mucosa harvest. This latter technique reduces postoperative pain, enhances intraoral soft-tissue mobility and reduces intraoral scarring. [54] Outcome Most authors mentioned in this review have reported excellent short-term outcome, viz., in the range of 70% to 90%. Singh et al., reported a success rate of 86.0% with dorsal onlay mucosal grafts. [55] In a comparative analysis of 63 patients and a mean follow-up at 55 months, BMG proved superior to flaps with respective success rates of up to 80% for mucosal grafts and 67% for flaps. [56] The results of BMG should ultimately be evaluated by the long-term outcomes. Lozano et al., achieved a 90% success rate with bulbar structures over a 10-year period. [57] Slovav reported a good and lasting potency of 76.9% in patients with long and complex anterior urethral structures. [58] Several authors have also reported excellent long-term outcomes. [9],[10],[11],[12],[59] Conclusions There is mounting evidence to suggest that oral mucosa is emerging as the tissue of choice for urethral substitution, and this tissue is also replacing skin graft and flaps for salvage urethroplasty in a variety of complex and recurrent strictures or failed hypospadias and epispadias repairs. Reconstructive urologists and pediatric surgeons in developing countries should therefore be familiar with this versatile technique for urethral reconstruction.[60] References
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