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The treatment of balanitis xerotica obliterans

I. Depasquale

West Midlands Regional Plastic and Reconstructive Surgery Unit, Stourbridge, West Midlands, UK

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A.J. Park

West Midlands Regional Plastic and Reconstructive Surgery Unit, Stourbridge, West Midlands, UK

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A. Bracka

West Midlands Regional Plastic and Reconstructive Surgery Unit, Stourbridge, West Midlands, UK

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First published: 02 January 2002
Cited by: 148
A. Bracka, Wordsley Hospital, Stourbridge, West Midlands DY8 5QX, UK.

Introduction

Balanitis xerotica obliterans (BXO), first described in 1928 by Stuhmer, is now considered to be the male genital variant of lichen sclerosus et atrophicus (LSA). This common penile disease can involve the prepuce, the glans ( Fig. 1) or the urethra, either individually or in any combination. BXO was regarded as an exclusively adult disease until a case was documented in a 7‐year‐old boy in 1962 [1]. Further reports of prepubertal BXO followed during the 1970s and currently it is recognized as a common cause of acquired phimosis and meatal stenosis in schoolboys, and has even been identified in the first year of life (unpublished communication). It remains speculation as to whether this represents a genuine change in prevalence and behaviour of this disease, or merely greater clinical awareness and recognition.

image

Photograph of a patient with BXO affecting the foreskin and glans (a). In another patient the pointer highlights the typical white appearance of BXO meatal stricture (b).

The aetiology of BXO remains obscure. Genetic factors have been implicated in association with HLA subtypes [2], which may explain our observation of brothers, or of fathers and sons, presenting with this condition. Several publications [3, 4] including ours, noted an increased incidence of other auto‐immune type conditions (e.g. diabetes, vitiligo, alopecia), not only among patients, but also their close relatives. An infective aetiology has also been considered although initial studies on viruses [5], spirochetes [6] and acid‐fast bacilli [7] were inconclusive or unsubstantiated.

Clinical features

The clinical presentation and severity of BXO can vary markedly. The onset may be insidious, pursuing a chronic course over many years with few early symptoms, or it may behave aggressively with florid disease evident within weeks of onset. In mild early BXO, the patient may notice areas of greyish white discoloration on the glans or the moist inner layer of the foreskin. It may or may not be itchy, and at this stage it is frequently misdiagnosed as a candidal infection and treated to no avail with antifungal creams. The involved areas of skin coalesce or spread, becoming inelastic and prone to fissuring or haemorrhagic blistering during sexual activity. The frenulum often becomes contracted and circumferential involvement of the preputial aperture leads to a progressive fibrous phimosis, characterized by the typical whitish discoloration. In aggressive BXO disease the surface of the glans and inner prepuce may ulcerate, causing purulent discharge. Subsequent fibrosis may lead to dense fusion of the layers, thereby making a routine circumcision difficult or impossible. The intermittent ulceration of the glans is often histologically not specific, but eventually this chronic instability may progress to squamous cell carcinoma (SCC), which has a recognized association with BXO. For these reasons, circumcision of a severe BXO phimosis in which the glans cannot be inspected or in which there is an associated purulent discharge, should not be delegated to an inexperienced surgeon.

Urethral involvement starts at the meatus, with a tendency to form superficial adhesions between the meatal lips in the milder cases, and then the typical dense ivory‐white fibrosis in more severe disease ( Fig. 1b). Although traditionally it was thought that BXO did not progress beyond the navicular fossa, our extensive experience shows that in long‐standing disease, mucosal involvement and spongiofibrosis can spread proximally as far back as the prostate. However, it has not been found in bladder mucosa. Clinically the penile urethra may feel like a thickened cord on palpation, and on urethroscopy (when possible) the involved mucosa looks pale and ‘shaggy’, sometimes with focal areas of fissuring or ulceration. The proximal extent is usually well demarcated when in the penile urethra, although with more extensive bulbar extension of the disease, the mucosal changes may fade indistinctly and we have sometimes noted the appearance of minor mucosal ‘skip’ lesions beyond the apparent posterior limit. However, generally the disease seems to spread proximally from the meatus in a confluent manner.

With experience, the clinical picture of established BXO is almost unmistakable, although the differential diagnosis might include lichen planus, localized scleroderma, leukoplakia, vitiligo and the cutaneous rash of Lyme disease. Furthermore, on histological examination BXO presents a very characteristic picture. Hyperkeratosis is present and the epidermis is atrophic with thinning of the rete pegs. Vacuolar degeneration of the basal layer may be present. The papillary and reticular dermis present a ‘washed out’ appearance and dermal collagen forms a homogenous band at the dermal‐epithelial junction in conjunction with elastin fibres, to produce an amorphous hybrid substance [8]. Deep to this amorphous band, a chronic inflammatory cell infiltration is present, mainly from T cells [9].

Treatment

BXO has been managed both medically and surgically. Currently available medical treatment can provide useful palliation but is generally regarded to be of limited benefit. Topically applied and intralesionally injected steroids have been shown to arrest the progression of the disease and in some cases cause regression or resolution, particularly in childhood phimosis. A trial with clobetasol or mometasone cream can be considered for those patients with early disease who are keen to avoid circumcision. However, on ceasing treatment the disease process may resume [10, 11]. Topically applied testosterone has been reported to have a beneficial effect, but this type of treatment has not been pursued further [12].

The surgical options are more definitive, and have included circumcision, dilating or surgically correcting meatal stenosis, and various urethroplasty techniques. The carbon dioxide laser has been used as an alternative to incisional surgery to ablate BXO on the glans [13-15] and for the dilatation of proximal strictures [16, 17].

Because previous reports include few patients and use uncertain treatment regimens, we reviewed a large series of histologically confirmed cases of BXO operated on by the senior author (A.B.), to establish a treatment protocol. To date, the senior author has treated ≈ 700 patients for BXO and its sequelae; 522 of these patients, operated on between January 1984 and May 1998, were studied retrospectively by reviewing the case‐notes and the senior author's database ( Table 1). Those who had BXO as their main pathology were treated surgically, 82 (16%) patients were treated for hypospadias with concurrent BXO and 12 (2%) had treatment for SCC associated with BXO ( Table 1).

Table 1. The pathology and site of BXO in patients treated between 1984 and 1998
Pathology or site No. (%) of patients
Total 522
BXO main pathology 428 (82)
BXO with hypospadias 82 (16)
BXO with SCC 12 (2)
Site:
Limited to foreskin/glans 300 (57)
Involving meatus 21 (4)
Urethral 107 (20)

The age of presentation of BXO was difficult to assess because many of the patients were referred from other units, having undergone several previous procedures over many years. Thus we assessed the subset of patients presenting for primary surgical treatment by circumcision, which would give a more accurate assessment. In the 300 patients treated by circumcision the youngest was a 2‐year‐old boy and the eldest an 81‐year‐old man. The median age at presentation was 33 years, with the highest incidence in those aged 21–40 years (145 patients, 48%).

Of these 300 patients with BXO limited to the foreskin or glans penis only, 287 (96%) were treated by circumcision alone. The remaining 13 (4%) required concurrent surgical procedures, i.e. meatotomy or meatoplasty in five, urethroplasty using mucosal grafts in four and glans resurfacing in four.

Of the 287 patients who had the glans exposed by circumcision alone as the definitive treatment, the disease process was arrested and symptoms relieved in 276 (92%). BXO remained active in 11 (3.9%) patients, with development of glans ulceration requiring total glans resurfacing in five, and with urethral spread requiring urethroplasty in six. Surgery to correct meatal stenosis was undertaken in 21 (4%) patients in the form of meatotomy (13) or meatoplasty (eight).

In all, 107 (20%) patients underwent surgery for a BXO urethral stricture, with excision of the involved urethra and replacement with grafts, the choice of graft changing with our length of experience. Initially, in 42 (39%) of these cases, skin (genital or not) was used for substitution, and although the early results were good, there was an almost 90% stricture recurrence rate during a long‐term follow‐up. The other 65 patients (61%), plus the recurrences from the skin group, underwent reconstruction with buccal and/or bladder mucosa. There have been no BXO recurrences in these mucosal grafts to date.

Of those with BXO, 82 (16%) were identified among patients who were being treated for hypospadias problems. Of these 82, 29 (35%) were presenting late for primary repair because a hitherto asymptomatic hypospadias deformity had become troublesome. Fifty‐three (65%) were referred for salvage surgery having already undergone unsuccessful hypospadias repairs elsewhere. Most were adults with a long history of recurrent strictures and multiple hospitalizations. Our experience in managing these patients mirrors that in patients with no hypospadiac stricture, i.e. those repairs that used skin to reconstruct the urethra eventually stenosed, whereas those using mucosal grafts have remained free of recurrence.

Penile SCC was associated with BXO in 12 (2.3%) patients; of these, seven had been circumcised earlier for BXO whilst the other five had BXO in uncircumcised penises. These patients were treated by conservative resection, combined with reconstruction of a pseudo‐glans. One of these patients developed a BXO urethral stricture requiring urethroplasty; another developed metastatic spread of his carcinoma, requiring an inguinal lymph node block dissection.

Discussion

BXO can be treated in several ways; of the 300 patients treated by circumcision, in all but 12 (4%) this was the only intervention required, underlining the efficacy of this mode of treatment. BXO has a predilection for the warm, moist, urine‐exposed environment that exists under the foreskin. In removing the moist skin folds and allowing the glans epithelium to dry out, circumcision usually leads to either resolution or arrest in progression of the disease, and alleviation of the symptoms. Mild glans disease may revert to a normal appearance within 6 months, and with more severe involvement, resolution may continue for up to 2 years after circumcision, although some permanent atrophic scarring and discoloration may then remain. Several authors [18, 19] have suggested that total excision of the involved epithelium is an effective way of eliminating the risk of recurrence. However, in our experience the associated desiccating effect of circumcision also plays an important role, and we recommend that sufficient foreskin should therefore be removed to allow adequate exposure and drying out of the glans. We have noted recurrence of BXO when the circumcision has been very conservative, even though the clinically diseased skin was removed. Recurrence is also common when residual moist skin folds are unavoidable because of obesity. Even after radical circumcision, in the obese patient the shaft skin may roll up to form a pseudo‐foreskin as the penis invaginates into the pubic fat pad. In these patients, despite repeated surgery, the entire penile shaft skin may eventually be destroyed and therefore radical weight loss is a priority for these patients if they are to avoid becoming genital ‘cripples’.

In a minority of cases the glans continues to deteriorate despite adequate circumcision, and the patient may have recurrent blistering, fissuring or ulceration of the skin. Twelve such patients were treated with topical clobetasol cream applied twice daily to the glans, but on follow‐up they continued to have problems. Five of them had persistent instability and ulceration of the glans surface ( Fig. 2ab), which was effectively treated by complete resection of the glans epithelium and resurfacing with partial thickness skin grafts ( Fig. 2c,d). The other seven developed urethral strictures requiring urethroplasty with buccal mucosa; on follow‐up these patients remain well. The reason that skin grafts seem to be effective on the circumcised glans but not in the urethra is that in the former the skin remains dry.

image

Long‐term disfigurement and instability in a patient after an attempted circumcision in advanced BXO (a), with fusion between the foreskin and glans (b). (c,d) show the cosmetic and functional improvement 6 months after complete denuding and exteriorization of the glans, then resurfacing with partial thickness skin grafts from the thigh.

BXO is a common disease, yet its true incidence is not appreciated because most cases are cured by circumcision, and unfortunately many surgeons still fail to send their circumcision specimens for histology. This practice is becoming medicolegally indefensible in a litigation‐conscious society, where the clinical sequelae of BXO are often misinterpreted by the patient as surgical errors. It is important to recognize when an unretractile foreskin is the result of established BXO, as these patients may have already developed a buried corona or more extensive fusion between the foreskin and glans, thereby making circumcision a challenging procedure. Failure to fully separate the adhesions will not only compromise the aesthetic outcome of circumcision, but may lead to recurrent painful fissuring around the corona during sexual activity. Given also the possibility of concurrent meatal or urethral stricture, or of malignant transformation, circumcision in these patients should not be delegated to an unsupervised trainee surgeon. Indeed, in severe cases, primary referral to a plastic surgeon or reconstructive urologist may be advisable.

BXO involvement of the urethra presents the challenging objective of restoring adequate urinary flow whilst minimizing the risk of recurrence. Various treatments have been recommended for meatal stenosis. Topical or injected steroids have shown some benefit [1, 20] especially when used as an adjunct to other treatments [21]. A simple ventral slit in the terminal urethra followed by dilatation tends to cause a distal hypospadias deformity and often leads to recurrence. Meatoplasty has been claimed to achieve a better functional result and a more permanent treatment of the stenosis [22]. The carbon dioxide laser has been used to treat meatal stenosis by ablation and meatotomy [17], or circumferential vaporization [16], with encouraging results. In our experience meatal stenosis may respond well to the above modalities, provided that circumcision has also been performed, and that the disease process is still confined to the meatal margins. Unfortunately, re‐stenosis can be anticipated once there is established BXO in the distal urethra. Urethroscopy is therefore mandatory if symptoms or clinical examination are suggestive of spread into the urethra.

To treat established urethral disease, excision of the involved urethra and substitution urethroplasty is the modality of choice. Conservative management with repeated urethrotomies and dilatations only exacerbates the fibrosis and recurrence of the stricture is virtually inevitable [23]. There is consensus that the involved urethral segment should be excised, and that delay merely allows the disease to spread further proximally, thereby making the subsequent surgery more difficult.

Various ways of reconstructing the urethra have been tried, including the use of pedicled skin flaps or skin grafts [24]. Our management of the urethra with BXO will be discussed in more detail elsewhere but from an experience of ≈ 200 BXO strictures we can draw several conclusions.

First, the diseased segment of urethra should be excised and substituted, rather than augmented with inlay flaps or grafts. Second, substitution urethroplasty with either genital or extra‐genital skin grafts provides no cure. The short‐term results may be excellent, but if such patients are followed for long enough then recurrent BXO strictures are almost inevitable. Re‐stricturing commonly occurs within the first 2–3 years, but it may take longer, and we have noted recurrences up to 10 years later. In the early 1990s we therefore started to use mucosa for reconstruction, and to date have encountered no recurrent BXO in a mucosal substitution urethroplasty.

We prefer a two‐stage procedure where first the urethra is laid open, and the involved mucosa excised and replaced by a graft of buccal mucosa harvested from one or both cheeks. The urethra is reconstituted at a second operation ≈ 4 months later. If the length of urethra involved is too much to replace with buccal mucosa alone, then we use buccal mucosa for the terminal segment and at the second operation replace the remaining diseased urethra with tubed bladder mucosa.

In the hypospadias‐BXO group, most salvage referrals presented with recurring strictures resulting from various types of hypospadias repair that use skin for the neourethra. BXO was confirmed on histological examination and the problems rectified when mucosa was used instead. The many hypospadias patients with BXO are unlikely to represent any specific association between these conditions, but probably reflects referral patterns to the unit because of the senior author's interest in hypospadias salvage.

Various authors [25-28] have reported the association between BXO and SCC of the glans, although by what mechanism this occurs and whether this is a specific causal relationship remains unclear. Some regard BXO as an inherently premalignant condition, whereas others consider it an unspecific irritant focus, comparable with chronic scarring or ulceration that eventually progresses to a Marjolin's ulcer. In our series, 12 patients with BXO (2.3% of 522) presented with SCC (median age 61.5 years, range 32–79); five presented with SCC in an uncircumcised penis, but intriguingly in the other seven the carcinoma had developed despite a previous circumcision for BXO phimosis. Why SCC of the glans should develop years after BXO circumcision remains unanswered, although it is possible that undiagnosed carcinoma in situ was already established at the time of primary surgery. We recommend that suspicious or atypical areas of BXO should be biopsied to exclude malignant transformation, especially in patients aged over 30 years.

Our patients were managed surgically, usually by glansectomy alone, but combined with a conservative amputation of the distal shaft if there was tumour penetration through to the corporal heads. We routinely reconstruct a pseudo‐glans by resurfacing the corporal heads or the contoured amputation stump with a split‐thickness skin graft from the thigh. This gives excellent functional and cosmetic results without compromising survival. Metastatic spread of the carcinoma occurred in only one patient, who required block dissection of the groin and has had no subsequent problems. We are now convinced, after a 10‐year experience with conservative surgery, that the traditional mutilating operations described for penile carcinoma are unwarranted in stage 1 and 2 disease, and our rationale will be the subject of a separate publication.

We stress that radiotherapy is not a treatment option for carcinoma of the glans when associated with BXO, because BXO spreads aggressively and relentlessly in immuno‐compromised, irradiated tissues, leading to florid and extensive involvement of the external genital skin and of the urethra. The management of such cases is exceedingly difficult.

A suggested treatment protocol

This is probably the largest series of BXO to date and therefore we suggest a protocol for the surgical treatment of BXO as currently practised in our unit.

•If the condition, as observed clinically, is limited to the foreskin, then circumcision is curative and provides histological confirmation of the disease.

•If there is associated glans discoloration, but with no scarring, ulceration or fusion to the foreskin, simple circumcision is again likely to be curative.

•Potent topical steroid creams may be a useful adjunct to manage localized areas that are reluctant to settle after circumcision, but we regard steroids as palliative rather than curative.

•If the coronal sulcus is obliterated by adhesions and the remaining glans skin is in reasonable condition, then we recommend release of the buried coronal ridge by careful sharp dissection, and allowing healing by secondary re‐epithelialization of the raw area.

•If the glans is extensively scarred and disfigured, or if the surface remains unstable and symptomatic, then total resurfacing of the glans with healthy new skin is recommended. This improves the aesthetic appearance and should remove the risk of progression to SCC.

•If SCC of the glans occurs, it is best treated by conservative, reconstructive surgery; radiotherapy should be avoided.

•Meatal BXO may respond to minor surgery and topical steroids, but stenosis is likely to recur if there is already established involvement of the distal urethra.

•The treatment for urethral BXO is excision of the involved urethra and substitution with full thickness buccal mucosa, or a combination of buccal and bladder mucosa in more extensive disease.

Conclusion

We present a treatment protocol ( Table 2) reflecting the experience in our unit of treating > 500 patients with BXO over a 14‐year period. Because few cases have been reported to date there is little consistent advice on the treatment of this under‐diagnosed condition. The protocol provides a treatment plan for managing most cases of BXO. Whilst many straightforward cases could be managed in a general surgery environment, it should be recognized that the sequelae of BXO can be technically challenging, and a proportion of patients will benefit from the services of a reconstructive specialist.

Table 2. A protocol for managing BXO
BXO involvement Treatment
Limited to foreskin Circumcision ± release of adhesions
Histology
Topical steroids as an alternative if very mild/asymptomatic
Glans Mild/moderate: circumcision and observation (± topical steroids)
Severe: glans resurfacing
SCC: resection and reconstruction
Meatal Early: dilatation (± topical steroids)
Established: meatotomy/meatoplasty and urethroscopy
Urethral Excise BXO urethra and replace with mucosal graft
Short segment: buccal
Long segment: buccal and bladder

Authors

I. Depasquale, Senior House Officer.

A.J. Park, FRCS, Specialist Registrar.

A. Bracka, FRCS, Consultant in Genitourethral Plastic Surgery.

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