Acitretin for Severe Lichen Sclerosus of Male Genitalia: A Randomized, Placebo Controlled Study
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1 Acitretin for Severe Lichen Sclerosus of Male Genitalia: A Randomized, Placebo Controlled Study D. Ioannides, E. Lazaridou,* Z. Apalla, E. Sotiriou, S. Gregoriou and D. Rigopoulos From the First Department of Dermatology-Venereology, Aristotle University Medical School, Thessaloniki, and First Department of Dermatology, A. Sygros Hospital, University of Athens Medical School, Athens (SG, DR), Greece Purpose: Genital lichen sclerosus is a chronic inflammatory and fibrosclerotic disease associated with substantial morbidity. Acitretin has been reported to be of benefit in many dermatological indications including lichen sclerosus. We evaluated the efficacy and tolerability of acitretin for biopsy confirmed, severe lichen sclerosus of the male genitalia. Materials and Methods: A randomized, double-blind, placebo controlled study was performed in which 52 male patients with severe, long-standing lichen sclerosus were randomized in a 2:1 ratio to receive daily acitretin (35 mg) or placebo for 20 consecutive weeks. Followup lasted for 36 weeks from baseline. The primary end point was complete response of active lichen sclerosus as well as improvement of patient quality of life. Secondary end points were partial response and recurrence rates after treatment discontinuation. Results: A total of 49 patients completed the study and were eligible for statistical analysis. Complete response was achieved by 36.4% (12 of 33) of the acitretin group vs 6.3% (1 of 16) of the controls, while 36.4% (12 of 33) vs 12.5% (2 of 16) achieved partial resolution, respectively. Mean total clinical score of the acitretin group was significantly lower than that of the controls at week 20 [t (47) 4.146, p ], which was also accompanied by a significant improvement in mean Dermatology Life Quality Index score [t (32) 6,441, p ]. Acitretin was well tolerated and only minimal transient side effects were recorded. Conclusions: Acitretin is safe and effective for the management of severe, longstanding lichen sclerosus of the male genitalia. Study limitations included bias during clinical evaluation considering the expected side effects of acitretin. Abbreviations and Acronyms DLQI Dermatology Life Quality Index LS lichen sclerosus RAR retinoic acid receptors TCS total clinical score VAS visual analogue scale Submitted for publication July 12, Study received institutional ethical committee approval. * Correspondence: 133 Tsimiski St., , Thessaloniki, Greece (telephone: ; FAX: ; bethlaz@med.auth.gr). Key Words: acitretin, lichen sclerosus et atrophicus, male, randomized controlled trial, retinoids LICHEN sclerosus is a chronic inflammatory skin disorder that affects both genders, but the incidence of LS is lower in men than in women. There are 2 types of disease presentation, the first occurring in young boys and the second during the third to fourth decade of life. The lesions appear most commonly on the prepuce, coronal sulcus and glans penis. 1 3 The perimeatal area may also be involved, and postinflammatory scarring may lead to stenosis and obstruction causing dysuria and poor urinary stream, complications that frequently necessitate surgical management. 4,5 Patients often experience significant morbidity as a consequence of the intractable symptoms, physical scarring and psychosexual damage. In addition, there is an increased risk of penile squamous cell /10/ /0 Vol. 183, , April 2010 THE JOURNAL OF UROLOGY Printed in U.S.A by AMERICAN UROLOGICAL ASSOCIATION EDUCATION AND RESEARCH, INC. DOI: /j.juro
2 1396 ACITRETIN FOR SEVERE LICHEN SCLEROSUS OF MALE GENITALIA carcinoma in those individuals with long-standing disease. 6,7 The goals of LS treatment are relief of symptoms and discomfort, prevention of any or further anatomical changes and the putative prevention of malignant transformation. 8,9 Although many treatments have been suggested over the years, ultra potent and potent steroids still remain the optimal choice for adults. 3,4 Systemic retinoids have been used in the past with some success in complicated vulvar LS but the teratogenic risk limits their use, especially in women of childbearing age. 10,11 In the current randomized, placebo controlled study we assessed the efficacy and tolerability of systemic acitretin in severe, intractable cases of LS in men. PATIENTS AND METHODS The study was conducted in accordance with the Declaration of Helsinki between March 2006 and March Protocol received institutional ethical committee approval and patients provided written informed consent before undergoing any study related procedure. Eligibility requirements for enrollment were histologically confirmed, severe genital LS, resistant to topical treatment with ultra potent steroids (at least 1 therapeutic cycle of 3 months) and age older than 18 years. Severe LS was arbitrarily defined as a TCS of 9 or greater according to the rating scale listed in table 1. TCS represented the sum of 6 different rates which were the result of the assessment of 3 individual parameters (symptoms, signs, extent of lesions). Exclusion criteria were hypersensitivity to retinoids or capsule components, severe renal or hepatic function impairment, alcohol consumption, metabolic disorders (intractable hyperlipidemia, diabetes mellitus), history of pancreatitis and hypervitaminosis A. Patients on medications that interact with retinoids or interfere with the immune system were also excluded from study. Biopsy, laboratory investigation and clinical evaluation were performed at the screening visit, while randomization and treatment initiation were held at baseline (week 0). Of 54 patients evaluated 51 met the eligibility criteria for enrollment, and were randomized in a 2:1 ratio of 34 to systemic acitretin and 17 to placebo. An individual not involved in the trial performed randomization using a computer generated randomization scheme. All patients in the treatment arm of the protocol received 35 mg acitretin once daily for 20 consecutive weeks. The applied dose regimen was selected by comparison with the therapy of patients with psoriasis treated with acitretin. The control group received placebo capsules identical in size and color to the acitretin. Both groups were equivalent with regard to certain demographic factors (eg age, concomitant diseases and medication) and disease activity (based on mean TCS and mean DLQI scores) at baseline. Use of any other systemic or topical treatment for LS except for topical emollients was prohibited during the study. In addition, all previous medications for LS were discontinued at least 30 days before baseline. For ethical reasons after the end of the treatment phase (week 20) subjects on placebo switched to acitretin treatment. Followup visits were scheduled at weeks 8, 16 and 20 for both groups. The acitretin group had an extra visit at week 36 from baseline. At each visit all patients had a thorough clinical examination, always by the same masked physician who recorded disease severity based on a specific rating system which is analyzed further. During the consultation patients were asked to fill in the DLQI questionnaires, and provide clinical data about current disease activity or side effects and adverse events. Furthermore, they were asked to determine subjective impression of pain intensity using a 0 to 100 VAS in which 0 represented no pain and 100 represented unbearable pain. Routine chemistry tests including lipid profile and hepatic chemistry study were measured every 4 weeks during the first 20 weeks of the protocol as well as at the end of the study. Clinical parameters considered to assess patient TCS were soreness or/and tightening sensation, pain including burning or stinging sensation, atrophic features, hyperkeratotic features, secondary features and extent of lesions. Detailed data about the grading procedure are provided in table 1. The rates obtained from the first 2 parameters were based on patient personal information while the rates of the remaining 4 were based on physical examination. The TCS was obtained by adding the previously mentioned scores, and had a range between 0 (minimum score) and 18 (maximum score). Complete response was defined as TCS 0. Patients with remaining atrophic features but no other symptoms or signs of the disease were also classified as complete responders because atro- Table 1. Analysis of subjective and objective clinical parameters that contribute to final TCS Grade 0 Grade 1 Grade 2 Grade 3 Symptoms: Soreness or tightening None Mild Moderate Marked Pain (VAS)* Signs: Atrophic features None Mild Moderate Marked Hyperkeratotic features None Mild Moderate Marked Secondary features None More than 4 Extent of lesions None Glans penis or prepuce 2 of Glans penis, prepuce, coronal sulcus, penis shaft, perineum * Including stinging and/or burning sensation, measured with VAS (0 to 100 mm). Including erosions, ulcerations, edema and lichenification. 3 or More of previously mentioned sites
3 ACITRETIN FOR SEVERE LICHEN SCLEROSUS OF MALE GENITALIA 1397 phic features are considered nonreversible and remain inalterable despite the beneficial effect of any conservative therapeutic procedure. Partial response was defined as at least a 4-point reduction of TCS from baseline to week 20. The DLQI questionnaire was calculated by summing the scores of 10 questions resulting in a maximum of 30 and a minimum of 0. The higher the score, the more patient quality of life was impaired (0 to 1 no effect at all, 2 to 5 small effect, 6 to 10 moderate effect, 11 to 20 very large effect, 21 to 30 extremely large effect). The DLQI was analyzed further under the 6 headings of symptoms and feelings, daily activities, leisure, work, personal relationships and treatment. The type and intensity of side effects and adverse events were also recorded. An adverse event was characterized as serious when it resulted in death or prolonged hospitalization, endangered patient life, resulted in persistent or significant disability or incapacity, or resulted in cancer or in any important medical event. All other events were considered nonserious and were also recorded. For the statistical analysis we evaluated the difference between the mean TCS of the acitretin group vs placebo at week 20 using the t test for independent samples. The Kolmogorov-Smirnov test (p 0.05) was applied for testing normality of distribution for both variables and Levene s test was applied for testing equality of variances. The significance of the difference between mean DLQI estimated at baseline and at week 20 for the acitretin and placebo groups, respectively, was evaluated using the 2-tailed Student t test for paired samples. Mean values and 95% confidence intervals for TCS and DLQI at each study visit were estimated for both groups, as well as for the corresponding mean time to response. All data were analyzed with SPSS version RESULTS Overall 51 of the 54 patients initially evaluated met eligibility requirements for enrollment. A total of 49 patients (33 of the acitretin and 16 of the controls) completed the study and were eligible for statistical analysis. Two subjects, 1 on acitretin and 1 on placebo, withdrew from the study and were excluded from statistical analysis. The reason for withdrawal was disease associated complications (phimosis) which demanded surgical management. The flowchart in the figure includes patient disposition and highlights important points. Patient age was between 39 and 74 years (mean SD ) for the control group, and between 38 and 75 years ( ) for the treatment group. According to our data 36.4% (12 of 33) of the subjects on acitretin and 6.3% (12 of 16) of controls achieved a complete response at the end of the study treatment phase. Partial response was observed in 36.4% (12 of 33) of the treatment group and in 12.5% (2 of 16) of the placebo group. Disease remained stable in 21.2% (7 of 33) of the acitretin group and 31.3% (5 of 16) of the control group, while 6.1% (2 of 33) of individuals on acitretin and 50.0% (8 of 16) on Flowchart of disposition of study patients, reasons for withdrawal and important points. placebo experienced disease progression. Mean time to complete response was 20.0 weeks because none of the complete responders reached this level of remission before of the end of the treatment phase (week 20). Mean time to partial response was 16.7 weeks (SD 2.548, 95% CI ). Of the patients in the acitretin group who achieved a complete response at the end of the treatment phase 41.7% (5 of 12) maintained that level of response until week 36 while 58.3% (7 of 12) experienced disease progression with a mean TCS increase of 3.71 points (SD 0.488, 95% CI ). Correspondingly 33.3% (4 of 12) of the partial responders remained stable until week 36 and 66.7% (8 of 12) experienced deterioration with a mean TCS increase of 3.13 (SD 0.835, 95% CI ). Of the subjects with stable disease at week 20, 57.1% (4 of 7) did not experience any change until the end of the study while 42.9% (3 of 7) had an increase in mean TCS of 1.67 points (SD 0.577, 95% CI ).
4 1398 ACITRETIN FOR SEVERE LICHEN SCLEROSUS OF MALE GENITALIA With regard to mean TCS in the acitretin arm of the protocol a gradual decrease was recorded from 9.39 (SD 0.747, 95% CI ) at baseline to 7.94 (SD 1.171, 95% CI ) at week 8, and 6.00 (SD 2.487, 95% CI ) and 4.55 (SD 3.969, 95% CI ) at weeks 16 and 20, respectively. Treatment cessation resulted in a subsequent increase in mean TCS from 4.55 to 6.24 (SD 3.606, 95% CI ). Mean TCS of the placebo group was 9.25 (SD 0.577, 95% CI ), 9.56 (SD 0.964, 95% CI ), 9.25 (SD 1.732, 95% CI ) and 9.31 (SD 3.321, 95% CI ) at weeks 0, 8, 16 and 20, respectively. Mean TCS of the acitretin group at a 0.05 level of significance was significantly lower than that of the control group at week 20 [t (47) 4.146, p ]. With respect to the DLQI of patients on acitretin the mean score decreased from (SD 2.335, 95% CI ) at week 0 to 6.76 (SD 3.913, 95% CI ) at week 20, which reflects a statistically significant difference at the 0.05 level of significance [t (32) 6,441, p ]. A minimal reduction from (SD 2.407, 95% CI ) at week 0 to (SD 2.482, 95% CI ) at week 20 was also recorded in mean DLQI of the controls. However, statistical analysis indicated that at a 0.05 level of significance there was no significant difference between these rates [t(15) 1.360, p ]. The fluctuation of mean TCS and mean DLQI in both groups is presented in table 2. In addition to the expected/typical well-known side effects of acitretin, only minimal transient side effects were recorded. The treatment was well tolerated and no severe adverse events were reported. The drug associated side effects are summarized in table 3. Table 3. Drug associated side effects % Acitretin group (No./total No.): Cheilitis 75.8 (25/33) Skin peeling 48.5 (16/33) Pruritus 30.3 (10/33) Paronychia 24.2 (8/33) Hair shedding 21.2 (7/33) Rhinitis 21.2 (7/33) Gastrointestinal disturbances 9.1 (3/33) Moderate hyperlipidemia 42.4 (14/33) Slight increase in liver enzymes 27.3 (9/33) % Control group (No./total No.): Gastrointestinal disturbances 25.0 (4/16) Headaches 18.8 (3/16) Pruritus 12.5 (2/16) Fatigue 12.5 (2/16) Dizziness 12.5 (2/16) Arthralgias 6.3 (1/16) DISCUSSION The significantly higher percentage of complete and partial responders in the acitretin arm of the protocol compared to placebo combined with the significant decrease in mean TCS observed in the acitretin group clearly demonstrates the beneficial effect of acitretin in male patients with severe genital LS. Furthermore, our results indicate that the administration of acitretin resulted in considerable improvement in patient quality of life, especially in terms of personal relationships. There are some interesting points that we consider valuable. We observed that patients on acitretin achieved a complete or partial response late in the treatment phase of the study. Analytically none of the complete responders reached that level of remission before week 20, which raises the question of whether a longer therapeutic phase could result in a higher percentage of complete response. In addition, although the mean TCS of patients on acitretin was moderately increased 16 weeks after treatment discontinuation, it remained significantly lower than that at baseline. Thus, an important part of the beneficial effect of the medication was maintained for at least 16 weeks. Given the chronic and recurrent nature of the disease we can postulate that intermittent therapeutic schemes could represent an optimal strategy to maintain high levels of response and minimize side effects. The study was designed as a double-blind, placebo controlled trial. However, there is no doubt that complete avoidance of bias could not be achieved considering the typical side effects provoked by systemic retinoids. This study is not the first to introduce the therapeutic potential of retinoids in genital LS. Former case reports 10 as well as a randomized Table 2. Level of response in TCS and DLQI scores at each followup point Mean Baseline (SD) Mean Wk 8 (SD) Mean Wk 16 (SD) Mean Wk 20 (SD) Mean Wk 36 (SD) Acitretin: TCS 9.39 (0.747) 7.94 (1.171) 6.00 (2.487) 4.55 (3.969)* 6.24 (3.606) DLQI (2.335) (1.979) 8.12 (2.619) 6.76 (3.913) 7.76 (5.420) Placebo: TCS 9.25 (0.577) 9.56 (0.964) 9.25 (1.732) 9.31 (3.321)* DLQI (2.407) (2.250) (2.277) (3.324) * Mean TCS of acitretin group is significantly lower than that of control group at week 20 [t (47) 4.146, p ]. Mean DLQI of acitretin group at week 20 is significantly lower than at baseline [t (32) 6.441, p ].
5 ACITRETIN FOR SEVERE LICHEN SCLEROSUS OF MALE GENITALIA 1399 placebo controlled trial 11 have focused on acitretin as a therapeutic regimen for LS. However, in that trial investigators included only female patients with vulvar LS. Therefore, a direct comparison of those results with ours is not appropriate. However, despite the existing differences our results are in agreement with their findings. Specifically according to their data a significantly higher percentage of responders was observed in the acitretin group (64%, 14 of 22 patients) than the placebo group (25%, 6 of 24 patients). Etretinate and acitretin, also known as aromatic retinoids, belong to the second generation of retinoids, and are synthesized by replacing the cyclic end group of vitamin A with various substituted and nonsubstituted ring systems. In fact, acitretin represents an orally active metabolite of etretinate with potential antineoplastic, chemopreventive, antipsoriatic and embryotoxic properties but the exact mechanism of action remains unknown. Acitretin activates nuclear retinoic acid receptors, resulting in induction of cell differentiation, inhibition of cell proliferation and inhibition of tissue infiltration by inflammatory cells. Acitretin has also been demonstrated to inhibit growth, and induce apoptosis and differentiation of a variety of tumors including squamous cell carcinoma. 12,13 There are 3 classes of RAR, alpha (RAR- ), beta (RAR- ) and gamma (RAR- ). Previous studies using nonradioactive in situ hybridization on surgical specimens of patients with vulvar LS demonstrated a significantly lower expression of RAR- compared to normal skin while RAR- was over expressed. Abnormal balance between RAR- and RAR- expression is an important factor in the regulation of keratinocyte differentiation, and it has a crucial role in mediating various effects of RAR signal transduction. Indeed abnormal RAR expression has been proposed to contribute to the development of nonneoplastic epithelial disorders such as lichen sclerosus. Application of RAR selective retinoids such as acitretin could result in an improvement in LS by altering the balance of RAR expression, which could represent a reasonable explanation of the beneficial effect of acitretin in our patients. 14 CONCLUSIONS Our results provide enough evidence to conclude that acitretin is an effective and safe therapeutic option for severe LS of the male genitalia in that it decreases disease activity and improves quality of life. ACKNOWLEDGMENTS Agorasti Toka, Industrial Management Division, Aristotle University of Thessaloniki, contributed to the study design and assisted with statistical analysis. REFERENCES 1. Powell JJ and Wojnarowska F: Lichen sclerosus. Lancet 1999; 353: Tasker GL and Wojnarowska F: Lichen sclerosus. Clin Exp Dermatol 2003; 28: Neill SM, Tatnall FM, Cox NH et al: Guidelines for the management of lichen sclerosus. Br J Dermatol 2002; 147: Pugliese JM, Morey AF and Peterson AC: Lichen sclerosus: review of the literature and current recommendations for management. J Urol 2007; 178: Kulkarni S, Barbagli G, Kirpekar D et al: Lichen sclerosus of the male genitalia and urethra: surgical options and results in a multicenter international experience with 215 patients. Eur Urol 2009; 55: Carlson JA, Ambros R, Malfetano J et al: Vulvar lichen sclerosus and squamous cell carcinoma: a cohort, case control, and investigational study with historical perspective; implications for chronic inflammation and sclerosis in the development of neoplasia. Hum Pathol 1998; 29: Nasca MR, Innocenzi D and Micali G: Penile cancer among patients with genital lichen sclerosus. J Am Acad Dermatol 1999; 41: Cooper SM, Gao XH, Powell JJ et al: Does treatment of vulvar lichen sclerosus influence its prognosis? Arch Dermatol 2004; 140: Renaud-Vilmer C, Cavelier-Balloy B, Porcher R et al: Vulvar lichen sclerosus: effect of long-term topical application of a potent steroid on the course of the disease. Arch Dermatol 2004; 140: Niinimaki A, Kallioinen M and Oikarinen A: Etretinate reduces connective tissue degeneration in lichen sclerosus et atrophicus. Acta Derm Venereol 1989; 69: Bousema MT, Romppanen U, Geiger JM et al: Acitretin in the treatment of severe lichen sclerosus et atrophicus of the vulva: a double-blind, placebo-controlled study. J Am Acad Dermatol 1994; 30: Ran L, Tan W, Tan S et al: Effects of ATRA, acitretin and tazarotene on growth and apoptosis of Tca8113 cells. J Huazhong Univ Sci Technolog Med Sci 2005; 25: Lebwohl M, Tannis C and Carrasco D: Acitretin suppression of squamous cell carcinoma: case report and literature review. J Dermatolog Treat 2003; 14: Berger J, Telser A, Widschwendter M et al: Expression of retinoic acid receptors in nonneoplastic epithelial disorders of the vulva and normal vulvar skin. Int J Gynecol Pathol 2000; 19: 95.
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