Safety and Tolerability of Adjuvant Topical Tacrolimus Treatment in Boys with Lichen Sclerosus: A Prospective Phase 2 Study
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1 european urology 54 (2008) available at journal homepage: Pediatric Urology Safety and Tolerability of Adjuvant Topical Tacrolimus Treatment in Boys with Lichen Sclerosus: A Prospective Phase 2 Study Anne K. Ebert a, *, Wolfgang H. Rösch a, Thomas Vogt b a Department of Pediatric Urology, Klinik St. Hedwig, University of Regensburg, Germany b Department of Dermatology, University of Regensburg, Germany Article info Article history: Accepted March 11, 2008 Published online ahead of print on March 19, 2008 Keywords: Balanitis sclerotica obliterans BXO Childhood Lichen sclerosus et atrophicus Relapse Tacrolimus ointment Topical therapy Abstract Background: Management of lichen sclerosus (LS) in boys is still controversial. Although in most cases only the prepuce is affected, meatal and urethral involvement may require major surgical reconstruction with substantial morbidity. Objective: Because the frequency of such complicated courses is still unclear, an adjuvant postoperative treatment is highly desirable. Therefore, we addressed safety and tolerability of tacrolimus 0.1% ointment in the postoperative period. Design, Setting, and Participants: Among 222 penile surgeries, in 25 cases LS was confirmed histologically and 20 of those patients participated in the adjuvant treatment study. Moreover, 18 patients of the same cohort showed a lichenoid inflammatory reaction pattern suggestive of early but not fully established LS. Interventions and Measurements: Subsequent to the operation and after explicit information about off-label use, parents applied tacrolimus 0.1% ointment twice daily to the glans and the meatus for 3 wk in cases of proven LS. The 18 patients with possible early LS were followed up only without any treatment. Clinical follow-up was performed up to 13 mo (median). Results and Limitations: All 20 LS patients completed the topical treatment without any relevant side-effects. Two relapses occurred in the treatment group and were clinically cured with an additional 3-wk cycle of topical tacrolimus 0.1% ointment. None of the 18 early LS cases progressed to full-scale LS. Conclusions: This is the first study showing that tacrolimus 0.1% ointment applied immediately after surgery of fully established LS is a tolerable and most probably safe adjuvant novel treatment option. Because the therapy led to disease control in all treated individuals for >1 yr (median), this study establishes the groundwork for future trials with expanded treatment and follow-up periods to verify the true clinical benefit of tacrolimus in patients after LS surgery. Lichenoid tissue reactions suggestive of early LS seem to require no adjuvant treatment. # 2008 European Association of Urology. Published by Elsevier B.V. All rights reserved. * Corresponding author. Department of Pediatric Urology, University of Regensburg, Klinik St. Hedwig, Steinmetzstr. 1-3, Regensburg, Germany. Tel ; Fax: address: anne-karoline.ebert@barmherzige-regensburg.de (A.K. Ebert) /$ see back matter # 2008 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi: /j.eururo
2 european urology 54 (2008) Introduction The etiology, true incidence, and dynamic evolution of lichen sclerosus (LS), synonymous with balanitis sclerotica obliterans (BXO), in boys is still controversial and partly unknown. Genetic factors, autoimmune mechanisms, as well as recurrent local infection and trauma are considered responsible for its manifestation in children [1 5]. Despiteauniform clinical appearance, LS can be unpredictably progressive and cause significant morbidity with the need of major urethral and glandular surgical reconstruction [1,3]. Meatal location of LS might be claimed as a predictive factor, but incidence and chronology of meatal and glandular involvement are unclear [3,6]. For a long time, circumcision was mistaken as a cause for meatal or glandular involvement [1,6]. In a retrospective series of 41 children 56% had glandular and 37% meatal lesions [3]. Over a period of 12.5 mo, only half the children remained without recurrence after a simple circumcision [3]. In 22% of those children complex urethral and glandular reconstructions were needed [3]. Hence, because no approved clinical or histologic risk factors are established for predicting progression, adjuvant topical treatment after any LS surgery could be reasonable. In a previous study by Hennge and coworkers, topical tacrolimus ointment was safe and tolerable in established LS in adults and seemed to be effective to control the disease [7]. Therefore, we conducted a prospective pilot study in boys using tacrolimus 0.1% ointment subsequent to surgery in histologically confirmed LS as an adjuvant topical therapy regardless of the kind of surgery conducted. The aim of this phase 2 study was to determine the safety and tolerability of topical tacrolimus 0.1% ointment in this postoperative setting. 2. Patients and methods Between August 2005 and August 2007, 222 boys underwent a full-thickness foreskin excision in our Pediatric Urology Department. Irrespective of the reason for penile surgery, histopathology was performed by an expert dermatopathologist (T.V.), who identified and classified five distinct histologic patterns: (1) acute balanitis, that is, dermatitis pattern; (2) nonspecific chronic balanitis; (3) fibrosing phimosis; (4) lichenoid tissue reaction suggestive of early LS; and (5) fully developed LS. The criteria for differentiation between lichenoid tissue reaction and fully developed LS are shown in Table 1. Indications for foreskin removal were phimosis in 68%, fibrosing phimosis in 5%, acute balanitis with urinary retention in 1.4%, meatal stenosis in 1.8%, hypospadias repair in 23.4%, and concealed penis repair in 0.5%. All 25 patients with a full-scale LS were offered participation in the prospective pilot phase 2 study, but only 20 did so after extensive information was given to the parents. Parents were explicitly informed about off-label use and signed an informed consent. During a check-up in our outpatient clinic 3 wk after surgery, parents were instructed to apply tacrolimus 0.1% ointment twice daily to the glans and the meatus for 21 d in an amount that could be gently rubbed in within 2 3 min. Clinical follow-up started after local treatment with clinical examinations, photographic documentation, and urinary flow and sonographic residual urine measurements. All 18 boys with possible initial LS were followed up according the same regimen but without treatment (median: 17 mo; range: 8 20 mo). Complete response was defined as absence of clinical signs and subjective symptoms. We statistically analysed clinical risk factors for recurrence of LS using Cross Tabs, 2 2 Matrix; p 0.05 was considered as significant. The Statistical Package for Social Science (SPSS1 12.0) for Windows was applied. 3. Results Histopathologic diagnoses of all specimen are listed in Table 2. LS was preoperatively explicitly suspected in 26 patients (11.7%). In 25 patients fully Table 1 Histologic differences between early and fully developed lichen sclerosus Early LS Fully established LS Hyperkeratosis +/++ Epidermal atrophy (thinning) +/++/+++ Vacuolar alteration of basal keratinocytes +/++ +/++/+++ Subepidermal, lichen planus mimicking bandlike inflammatory +++ /+ lymphocytic infiltrate with variable epidermotropism (lichenoid tissue reaction) Deep LS typical, mid-dermal bandlike inflammatory lymphocytic infiltrate +++ Subepidermal edema +++ Homogenisation and sclerosis of subepidermal collagen +++ Dilated thin-walled vessels, haemorrhage +++ LS = lichen sclerosus.. + present; not present; / or.
3 934 european urology 54 (2008) Table 2 Histopathologic findings among 222 consecutive prepuces Acute balanitis, that is, dermatitis pattern 8 (3.6%) Nonspecific chronic balanitis 8 (3.6%) Fibrosing phimosis 8 (3.6%) Lichenoid tissue reaction suggestive of 18 (8.1%) early lichen sclerosus Fully developed lichen sclerosus 25 (11.3%) Normal preputial histopathology 155 (69.8%) developed LS was confirmed histologically (11.3%), another 18 patients showed a lichenoid tissue reaction suggestive for early LS, type 4 (8.1%). Sensitivity of clinical assessment of LS was 68%, whereas specificity was 95.6%. All 20 boys who participated in the study (mean age: 9.7 yr; range: yr) finished topical treatment without clinically relevant side-effects; follow-up is now a median 13 mo (range: 8 28 mo). Clinical diagnoses were phimosis in 15 (75%), hypospadias in 4 (20%), and meatal stenosis in 1 patient (5%). In 75%, preoperatively suspected LS could be confirmed histologically. In 25%, LS was found histologically without apparent clinical correlates. In these 20 patients, 4 hypospadias repairs (20%), 12 complete circumcisions (60%), 3 incomplete circumcisions (15%), and 1 meatotomy with redo circumcision (5%) were performed, so that in all cases sufficient foreskin material for subsequent histopathologic work-up could be obtained. Prior to surgery topical treatment with clobetasone butyrate 0.05% was applied to resolve phimosis without success in eight of the boys; seven received topical cortisone exclusively and one boy, after failure of initial cortisone treatment, tacrolimus 0.03% ointment due to his parents initial strict denial of circumcision. Clinically, LS was located at the prepuce exclusively in 11 boys (55%), additionally to the prepuce at the glans in 3 (15%), additionally at the meatus in 4 (20%), and simultaneously at the glans and the meatus in 2 (10%). Thus, in nine included patients (45%) minimal LS lesions were left, that is, the subsequent topical treatment was in true terms not only adjuvant but partially therapeutic plus adjuvant. In all those patients with minimal residual LS after surgery a full clearing of all visible signs was achieved after 3 wk of adjuvant treatment. In one 14.3-year-old boy from this group a whitish glandular LS recurrence was discovered 6 mo after circumcision. Although he lacked voiding symptoms, he complained of itching and decreased glandular sensation. Tacrolimus 0.1% ointment was again applied to the glans for another 3 wk. For 6 mo now his glans is completely cleared and the peak urinary flow rate is 28 ml/s without any residual urine. In the 11 patients with true adjuvant treatment, that is, no more clinical signs of LS after surgery, we also observed one relapse (9%), whereas 10 had continued full remissions up to a median of 12.7 mo. This 8.2-year-old boy suffered from voiding difficulties and dysuria 8 mo after circumcision. Obstructive urinary flow pattern and significant residual urine (80 ml) confirmed relevant inflamed meatal stenosis on clinical examination. After one more 3-wk cycle of tacrolimus 0.1%, voiding dysfunction and complaints disappeared. For 8 mo he has been stable, with a wide meatus and good urinary flow rate (peak 18 ml/s) without residual urine. No adverse events such as sensations of burning, severe itching, or erythema were reported. Only mild initial itching at the glans was reported by four patients (20%). However, Itching ceased spontaneously in all children and no additional supportive treatment or discontinuance of therapy was necessary. Because one further aim of the study was to identify possible predictors of relapse risk, we also analysed the correlation between preoperative LS suspicion, age, manifestation site, previous topical therapy, and relapse events. However, probably due to the low numbers of relapse events after therapy, no significant correlations were detected. All patients with possible early LS, that is, a lichenoid tissue reaction (Table 1), were closely followed up without treatment; interestingly these patients were younger than the group with fully established LS (median age: 4.8 yr; range: yr). Compared to fully developed LS this was mainly a histopathologic coincidence finding (88.9%); 77.8% of them presented as a bland phimosis and 22.2% as an unsuspicious hypospadias. Only in two cases was LS also clinically suspected (11.1%). Topical clobetasone butyrate 0.05% was applied to resolve phimosis in six patients, which initially failed in four and relapsed in two after initial successful cortisone treatment (11.1%). Seven (38.9%) complete and 11 (61.1%) partial circumcisions were performed. During median follow-up of 17 mo, no clinical recurrence at the foreskin, glans, or meatus occurred in this subset of patients. Urinary flow rates were measured with a median 15.8 ml (range: 8 35 ml/s); 91% of the patients did not have residual urine and only one boy had a voiding dysfunction with 50 ml residual urine. 4. Discussion Multicentre randomised studies have documented safe and possibly efficient long- and short-term
4 european urology 54 (2008) topical tacrolimus treatment of LS in both sexes, but mainly adults [7,8]. In a recent phase 2 study, 43% of the patients had a total and 34% a partial clearance of LS lesions, and in 9% recurrences were observed during follow-up [7]. The time to clearance varied considerably between 10 and 24 wk and total application periods ranged from 1.5 to 10 mo, respectively [7 11]. These therapeutic studies underline the potential effectiveness of tacrolimus in LS and make it a good candidate for the postsurgical concept proposed in this adjuvant phase 2 study. Variable clinical competence as well as varying frequency of histologic foreskin examinations are probably the reason for the considerable range of incidence numbers given in the literature. Ten to 95% of the boys undergoing penile surgery were reported to have LS [1,3,4,6,12,13]. Unfortunately, from those previous data no histopathologic or clinically markers can be extracted to predict the risk for potential disease progression or persistence or postoperative morbidity. Therefore, an adjuvant treatment option that bears a low risk for the patients is highly desirable. However, the need for adjuvant postoperative therapy of LS has been questioned by plastic and urologic surgeons [1,2,6,14]. A radical operative attempt including complete surgical excision of the inner foreskin and even tangential abrasion of glandular lesions was expected to be curative [2,13,14,15]. Drying out the glans was believed to play a major role, and some studies reported low recurrence rates of about 4% after radical circumcision [2]. Moreover, in a small series of 10 LS cases the chance for spontaneous regression of glandular lesions after radical circumcision without further treatment was estimated to be >60% within 5 yr [14]. On the other hand, some studies support a trauma theory and the isomorphic phenomenon, that is, LS was not rarely seen after surgery conducted for reasons other than LS [6]. Moreover, adjuvant treatment seems desirable in meatal and glandular involvement, which is considered as possible risk factor for complicated clinical courses. Meatal and glandular involvement is often discovered not earlier than after complete healing of circumcision wounds [6,15]. Most remarkably, in our series 45% of full-scale LS patients had glandular or meatal involvement. This demonstrates that, whatever radical surgical approach is performed, it might not be completely curative. In these circumstances potential recurrence rates are estimated to be high because the meatal or urethral target is still exposed to underlying immunologic conditions [4]. The common adjuvant and therapeutic principle is the use of topical corticosteroids. Complications in LS management seem to be less frequent when adjuvant steroidal treatment was applied early, latency periods to diagnosis were shorter and affected skin areas were smaller [3,4,6,13,16,17]. Since 2003, tacrolimus (FK506), an innovative immunosuppressive agent, has been used as a systemic drug to prevent organ rejection after allogenic transplantation and has been used as topically active 1% ointment in several conditions [7 11]. Due to its macrolide-like structure, permeation and absorption to the upper dermal segment are optimal without the typical steroid-like atrophogenic or rebound effects. Tacrolimus inhibits calcineurin, a phosphatase relevant for gene transcription of activated T lymphocytes, early T-cell activation, and proinflammatory cytokine production of interleukin 2 and tumor necrosis factor a [11]. Tacrolimus does not interfere with keratinocyte proliferation or collagen synthesis but stabilises mast cells and reduces antigen-presenting Langerhans cells [11]. Systemic absorption of tacrolimus seems to be very low and without clinical significance. Although there is a theoretically assumable risk of malignancy due to local immunosuppression in topical therapy, there is no single case of cancer reported that is convincingly related to topical therapy. Meanwhile several hundred thousands of years of therapy have been dispensed [7 11]. In Germany, topical tacrolimus is licensed for atopic eczema in adults (0.1%) and children (0.03%) after the second year of life for up to two thirds of the body surface, if other topical medications are not sufficiently effective or contraindicated. In persons younger than 16 yr therapy should be discontinued after 3 wk. In our prospective adjuvant pilot study tacrolimus 0.1% ointment was applied to the regions at risk (glans and meatus), irrespective of the surgical approach in histopathologically confirmed LS. Due to the adjuvant setting the application period was significantly shorter than former therapeutic protocols of active LS [7]. Most importantly, this is the first study showing that adjuvant treatment with tacrolimus ointment administered postoperatively is safe and tolerable. In 20% only temporary mild-to-moderate, self-limiting itching was experienced after applying tacrolimus 0.1% ointment. Interestingly, in the partially therapeutic setting subtle postoperative glandular and meatal residuals disappeared after 3 wk of topical tacrolimus treatment. Nevertheless, 10% had recurrences after 6 and 8 mo despite the single-cycle treatment with tacrolimus. This raises the question whether
5 936 european urology 54 (2008) prolonged adjuvant treatment, for example, 6 10 wk, would have been more favourable [7]. In addition, regular follow-up can help to detect the recurrences early. In our experience, in those two cases a repeated 3-wk cycle with topical tacrolimus led to complete clearance. In contrast to our former disease management algorithms, no additional surgical intervention was necessary [9]. Moreover, when doing a historical control we could collect evidence for a trend to fewer recurrences after topical tacrolimus compared to standard treatment with topical corticosteroids [9]. Therefore, taken together, we think the emerging evidence of this study sufficiently justifies further prospective randomised protocols to define the true postoperative effectiveness of topical tacrolimus versus cortisone treatment in boys with histologically confirmed fully established LS to control relapses and disease progression. Currently, LS histology is perceived as a spectrum ranging from distinct early changes without severe fibrosis to full-scale LS. In early lesions of LS the infiltrate can be quite heavy, superficial, and bandlike, possibly mimicking lichen planus. Basal apoptosis and vacuolar change are also features of this condition, described herein as lichenoid tissue reaction (Table 1). It is still an open question how frequently such lichenoid inflammatory conditions will progress to a full-scale LS with major degeneration of the connective tissue in the upper dermis. In this context, it is an interesting observation of our study that all 18 patients with such early lichenoid tissue reactions were younger than the boys in the LS group and had an excellent prognosis without adjuvant treatment. Therefore, we would not recommend uncritical application of tacrolimus as an adjuvant therapy in boys with this type of lichenoid reaction. 5. Conclusions Tacrolimus 0.1% ointment is a safe and tolerable adjuvant option after surgery of LS, particularly if there is a risk of complicated outcome due to meatal or glandular involvement. Further controlled trials comparing tacrolimus to placebo and potent topical steroids are necessary to prove the effectiveness in postoperative adjuvant treatment of LS in children. Author contributions: Anne K. Ebert 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: Ebert, Rösch, Vogt. Acquisition of data: Ebert, Rösch. Analysis and interpretation of data: Ebert, Vogt. Drafting of the manuscript: Ebert, Vogt. Critical revision of the manuscript for important intellectual content: Ebert, Rösch, Vogt. Statistical analysis: Ebert. Obtaining funding: NA. Administrative, technical, or material support: NA. Supervision: Rösch, Vogt. Other (specify): None. 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: Financially supported by Astellas Pharma GmbH. Funding/Support and role of the sponsor: None. References [1] Das S, Tunuguntla HS. Balanitis xerotica obliterans a review. World J Urol 2000;18: [2] Depasquale I, Park AJ, Bracka A. The treatment of balanitis xerotica obliterans. BJU Int 2000;86: [3] Gargollo PC, Kozakewich HP, Bauer SB, et al. Balanitis xerotica obliterans in boys. J Urol 2005;174: [4] Mattioli G, Repetto P, Carlini C, Granata C, Gambini C, Jasonni V. Lichen sclerosus et atrophicus in children with phimosis and hypospadias. Pediatr Surg Int 2002;18: [5] Powell J, Wojnarowska F, Winsey S, Marren P, Welsh K. Lichen sclerosus premenarche: autoimmunity and immunogenetics. Br J Dermatol 2000;142: [6] Meffert JJ, Davis BM, Grimwood RE. Lichen sclerosus. J Am Acad Dermatol 1995;32: [7] Hennge UR, Krause W, Hofmann H, et al. Multicentre, phase II trial on safety and efficacy of topical tacrolimus ointment for the treatment of lichen sclerosus. Br J Dermatol 2006;155: [8] Ginarte M, Toribio J. Vulvar lichen sclerosus successfully treated with topical tacrolimus. Eur J Obstet Gynecol Reprod Biol 2005;123: [9] Ebert AK, Vogt T, Rösch WH. Die topische Therapie der Balanitis xerotica obliterans (BXO) im Kindesalter: Klinische Langzeitergebnisse und Übersicht. Urologe 2007;46: [10] Böhm M, Frieling U, Luger A, Bonsmann G. Successful treatment of anogenital lichen sclerosus with topical tacrolimus. Arch Dermatol 2003;139: [11] Rallis E, Korfitis C, Gregoriou S, Rigopoulos D. Assigning new roles to topical tacrolimus. Expert Opin Investig Drugs 2007;16: [12] Clemmensen OJ, Krogh J, Petri M. The histologic spectrum of prepuces from patients with phimosis. Am J Dermatopathol 1988;10: [13] McLelland J. Lichen sclerosus in children. J Obstet Gynaecol 2004;24:733 5.
6 european urology 54 (2008) [14] Meuli M, Birner J, Hanimann B, Sacher P. Lichen sclerosus et atrophicus causing phimosis in boys: a prospective study with 5-year follow-up after complete circumcision. J Urol 1994;152: [15] Herschorn S, Colapinto V. Balanitis xerotica obliterans involving anterior urethra. Urology 1979;14: [16] Vincent MV, Mackinnon E. The response of clinical balanitis xerotica obliterans to the application of topical steroid-based creams. J Pediatr Surg 2005;40: [17] Fischer G, Rogers M. Treatment of childhood vulvar lichen sclerosus with potent topical corticosteroid. Pediatr Dermatol 1997;14: Editorial Comment on: Safety and Tolerability of Adjuvant Topical Tacrolimus Treatment in Boys with Lichen Sclerosus: A Prospective Phase 2 Study Guido Barbagli a, Massimo Lazzeri b a Center for Reconstructive Urethral Surgery, Arezzo, Italy b Department of Urology, Santa Chiara Hospital (GIOMI group), Florence, Italy lazzeri.m@tiscali.it Ebert and coworkers addressed the safety and tolerability of tacrolimus 0.1% ointment in the postoperative management of boys who underwent a full-thickness foreskin excision for penile lichen sclerosus (LS). This article deals with a challenging topic, as the urologic literature is lacking data and does not provide protocols for the treatment of LS [1]. What does the urologist need to know about LS? 1. In 1995, the prestigious American Academy of Dermatology recommended that the term lichen sclerosus, instead of balanitis xerotica obliterans, be used in future reports to emphasize its incidence and its malignant potential [2]. 2. LS is a precancerous lesion. The incidence of neoplastic changes among patients with LS ranges from 2.3% to 8.4% [3]. Patients with LS should be observed closely to detect neoplastic lesions as early as possible, and biopsy of any area of induration should be performed [3]. 3. The incidence of urethral strictures in patients with LS remains uncertain. Patients with failed hypospadias repair showed a high incidence of LS [4,5]. This is another open question. 4. The use of topical corticosteroid agents is beneficial in the acute phase of LS, because they may stop skin itching and reddening. The results of the topical therapy, presented by Ebert and colleagues in this article of European Urology, are encouraging, but further studies on a large series of patients are necessary to better clarify which patients should be treated using medical and not surgical therapy [1]. 5. To sum up, LS is a complex, aggressive immunological disorder involving the male genitalia and urethra. LS presents challenges for the urologist, because there are no effective medical therapies and the results of surgery are often frustrating. LS can be a tragedy for the patient, destroying patient quality of life, because it involves urinary and sexual functions and the aesthetic appearance of genitalia. At present, no medical or surgical therapies can restore the integrity of the genitalia affected by LS, and urologists need to follow up patients for years in order to provide an early diagnosis of neoplastic lesions. References [1] Ebert AK, Rösch WH, Vogt T. Safety and tolerability of adjuvant topical tacrolimus treatment in boys with lichen sclerosus: a prospective phase 2 study. Eur Urol 2008;54: [2] Powell JJ, Wojnarowska F. Lichen sclerosus. Lancet 1999;353: [3] Palminteri E, Berdondini E, Lazzeri M, Mirri F, Barbagli G. Resurfacing and reconstruction of the glans penis. Eur Urol 2007;52: [4] Barbagli G, De Angelis M, Palminetri E, Lazzeri M. Failed hypospadias repair presenting in adults. Eur Urol 2006;49: [5] Bracka A. Editorial comment. Eur Urol 2006;49:895. DOI: /j.eururo DOI of original article: /j.eururo
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