Lichen Sclerosus and Isolated Bulbar Urethral Stricture Disease
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1 Lichen Sclerosus and Isolated Bulbar Urethral Stricture Disease Joceline S. Liu,* Kelly Walker, Daniel Stein, Sanjiv Prabhu, Matthias D. Hofer, Justin Han, Ximing J. Yang and Chris M. Gonzalez Departments of Urology and Pathology (SP, XJY), Northwestern University Feinberg School of Medicine, Chicago, Illinois Purpose: Lichen sclerosus is a chronic inflammatory genital skin condition that can cause destructive urethral scarring. To our knowledge no prior study has described lichen sclerosus in isolated bulbar urethral stricture segments without progressive disease originating from the penile urethra. We report the incidence of lichen sclerosus in isolated bulbar urethral stricture segments. Materials and Methods: We retrospectively reviewed the records of 70 patients after urethroplasty for isolated bulbar stricture disease was performed from 2007 to Stricture specimens were re-reviewed by a single uropathologist. Cases were evaluated using common histological features of lichen sclerosus, including hyperkeratosis or epithelial atrophy, basal cell vacuolar degeneration, lichenoid lymphocytic infiltrate and superepithelial sclerosis. Results: Average patient age was 46.5 years (range 19 to 77) and average stricture length was 3.5 cm (range 1 to 7). Of the patients 51 (73.0%) underwent excision and primary anastomosis, and 19 (27.1%) underwent buccal mucosal onlay. In 6 patients (8.6%) stricture recurred during a median followup of 22 months (IQR 14, 44). Three of those patients had lichen sclerosus. Initial pathology assessment revealed lichen sclerosus in 5 patients (7.1%, 95% CI 1.0e13.3). On re-review of specimens using pathology criteria specific to lichen sclerosus 31 patients (44.3%, 95% CI 32.4e56.2) showed pathology findings highly suggestive of (13) or diagnostic for (18) lichen sclerosus (p ¼ ). On pathological re-review lichen sclerosus was associated with recurrent stricture. Conclusions: On re-review of surgical specimens we noted a significant incidence of lichen sclerosus in isolated bulbar strictures in men undergoing urethroplasty. The incidence of lichen sclerosus may be higher than reported in isolated bulbar urethral segments without evidence of distal to proximal progressive urethral disease. Abbreviations and Acronyms EPA ¼ end primary anastomosis LS ¼ lichen sclerosus Accepted for publication March 13, * Correspondence: 303 East Chicago Ave., Tarry 16, Chicago, Illinois (telephone: ; FAX: ; jocelineliu@northwestern.edu). See Editorial on page 636. Key Words: urethra; constriction, pathologic; lichen sclerosus et atrophicus; incidental findings; anatomy LICHEN sclerosus is a chronic inflammatory skin condition commonly involving the anogenital area. 1 LS can cause destructive genitourinary scarring and it confers an increased risk of penile squamous cell carcinoma although a causal relationship remains to be established. 2 In men with urethral stricture the incidence of urethral LS is reported to be between 4.8% and 14%. 3 In contrast to urethral stricture of other etiologies, LS related urethral strictures have a higher rate of treatment related morbidity and disease recurrence, which necessitates accurate /14/ /0 THE JOURNAL OF UROLOGY 2014 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION AND RESEARCH,INC. Vol. 192, , September 2014 Printed in U.S.A. j 775
2 776 LICHEN SCLEROSUS AND ISOLATED BULBAR URETHRAL STRICTURE DISEASE diagnosis and staging to plan appropriate management. 4 While LS treatment limited to the glans and urethral meatus has acceptable outcomes with minimally invasive approaches such as circumcision and meatotomy, more extensive or panurethral disease warrants more invasive therapy, including 1-stage oral graft urethroplasty vs staged urethroplasty with nongenital skin or oral mucosa. 5e7 Urethral LS is thought to originate at the meatus and/or preputial skin with potential disease progression proximally along the urethra. 7 The progressive proximal spread of LS is believed to result from a combination of embryological factors with disease extension through urethral glands or transformation of disease secondary to high pressure voiding and urethral inflammation. 8,9 To our knowledge no prior group has reported LS in isolated bulbar urethral stricture segments without progressive disease extending from the penile urethra or glans. We report the incidence of LS in isolated bulbar urethral stricture segments on re-review of bulbar urethroplasty specimens. We hypothesized that the incidence of LS involvement in isolated bulbar urethral stricture disease has been underreported to date. histological features in LS, including 1) hyperkeratosis, 2) thinning or thickening of the epidermis or squamous epithelium, 3) attenuation or vacuolar degeneration of the basal cell layer, 4) subepithelial hyalinization/dermal collagen homogenization and 5) lichenoid lymphocytic or plasmacytic infiltrate. 10,11 While each individual finding is suggestive of LS, the combination of these pathological features is the basis of the pathological diagnosis of LS. 12 There is no gold standard of objective criteria for systematically evaluating LS. Recently new diagnostic pathological criteria were developed for LS in which cases with 0 or 1 features were deemed negative for LS, cases with 2 features were deemed suggestive of LS and cases with 3 or more features were deemed diagnostic for LS. 13 Using the Student t-test we compared the incidence of LS on original pathology results based on review of the medical record pathology report and on specimen re-review categorized as pathology findings suggestive or diagnostic of LS based on the described scheme. 13 Characteristics were compared between patients with vs without LS on re-review of pathology slides using the Mann-Whitney U and Fisher exact tests. Recurrence was defined by patient reported urinary symptoms confirmed by endoscopic diagnosis of recurrent urethral stricture 16Fr or less in caliber. The recurrence rate was compared between patients with and without LS on re-review using the chi-square test. For all statistical analyses p <0.05 was considered statistically significant. Analysis was done with SPSSÒ, version 21. MATERIALS AND METHODS We performed an institutional review board approved, retrospective study of patients who underwent urethroplasty for isolated bulbar stricture disease at a single institution between 2007 and Isolated bulbar urethral stricture was defined based on intraoperative findings with stricture disease limited to the urethra proximal to the penoscrotal junction and distal to the sphincter. Patients with less than 1 year of followup, history of LS involvement of the more distal penile urethra and meatus or a history of urethral trauma (ie straddle injury, urethral disruption or tear, pelvic fracture) were excluded from analysis. The final study cohort included 70 patients. Patient data were retrospectively gathered from electronic medical records. Demographic information, etiology, comorbidities, smoking history, prior procedures, surgical intervention, outcomes and pathology findings were reviewed based on inpatient and outpatient history, and physical, problem list and progress notes. Initial surgical pathology results of the excised stricture were reviewed from the electronic medical records and categorized according to the original pathological diagnosis. At our institution we routinely encounter and excise the stricture during EPA or a small sample of scar tissue at the cut edges of the urethrotomy during onlay urethroplasty and send it for pathological analysis. Stricture specimens at urethroplasty were retrospectively reviewed by a single uropathologist (XJY) blinded to patient history and prior histopathological diagnoses. Slides stained with hematoxylin and eosin were requested and obtained. Cases were evaluated using 5 common RESULTS A total of 70 men with an average age of 46.5 years (range 19 to 77) underwent bulbar urethroplasty for isolated bulbar stricture disease with no history of urethral trauma and at least 1 year of followup. Average urethral stricture length was 3.5 cm (range 1 to 7). Ten patients (14.2%) had a smoking history and 43 (61.4%) had undergone prior intervention for stricture, including urethroplasty in 3 (4.3%) and hypospadias repair related urethral complications in 5 (7.1%). EPA was performed in 51 patients (73.0%), and 18 (25.7%) and 1 (1.4%) underwent dorsal and ventral onlay of buccal mucosal graft, respectively. Initial surgical pathology reports mentioned LS involvement in 5 patients (7.1%, 95% CI 1.0e13.3) with findings suggestive of LS in 1 (1.4%) and a LS diagnosis in 4 (5.7%). On re-review of pathology slides in blinded fashion by a single, specialized uropathologist using the previously described diagnostic criteria patients (44.3%, 95% CI 32.4e56.2) fulfilled pathology criteria for LS. Of these 31 patients pathology findings were highly suggestive for LS in 13 (18.6%) and diagnostic for LS in 18 (25.7%) (fig. 1). Figure 2 shows representative sections highlighting characteristic histopathological findings of LS. The incidence of LS on the initial pathology report compared to re-review differed significantly
3 LICHEN SCLEROSUS AND ISOLATED BULBAR URETHRAL STRICTURE DISEASE 777 Patient characteristics with or without pathological evidence of LS on re-review Av No LS (95% CI) Av LS (95% CI) p Value* Figure 1. LS incidence at initial pathology evaluation and re-review. Based on number of identified characteristic histopathological findings in LS cases were further categorized with pathology results suggestive (hatched bars) or diagnostic (diamond bars) of LS. (p ¼ ). No statistically significant difference was noted between patients with and without LS on re-review, although those with a history of failed intervention such as hypospadias repair or urethroplasty showed a trend toward LS pathology findings on re-review (p ¼ 0.08, see table). Stricture recurrence requiring intervention developed in 6 patients (8.6%) at a median followup of 22 months (IQR 14, 44). Average stricture length was 3.5 cm (95% CI 3.1e3.8) in patients without recurrence vs 4.3 cm (95% CI 2.7e5.8) in those with recurrence. Preoperative stricture length did not statistically differ in patients with and without recurrence (p ¼ 0.21). Five patients underwent buccal mucosal graft onlay while 1 underwent EPA. The recurrence site was distal relative to urethroplasty in 3 patients, proximal in 2 and unknown in 1 who underwent cystoscopy performed by a Figure 2. Two cases considered diagnostic for LS. A, prominent histopathological features include basal layer degeneration (asterisk) and chronic lichenoid inflammatory infiltrate (arrow). B, hyperkeratosis (star), epithelial attenuation (arrowhead) and subepithelial hyalinization (x) were present. H&E, reduced from 10. No. pts e Stricture length (cm) 3.4 (2.9e4.0) 3.7 (3.2e4.1) 0.35 Followup (mos) 26.8 (21.0e32.6) 30.7 (23.8e37.5) 0.28 Age: 47.7 (17.9) 45.5 (18.0) 0.57 % Less than (13.4e43.0) 19.4 (4.6e34.1) 0.4 %30eLess than (5.4e30.6) 16.1 (2.4e29.8) 0.84 %40eLess than (1.8e23.8) 12.9 (0.4e25.4) 0.99 %50eLess than (7.3e33.8) 19.4 (4.6e34.1) 0.9 % (7.3e33.8) 32.3 (14.8e49.7) 0.26 % History: Diabetes mellitus 15.0 (4.0e27.0) 10.0 (0.0e21.0) 0.72 Smoking 10.0 (0.0e20.0) 19.0 (5.0e34.0) 0.32 Radiation 5.0 (0.0e12.0) 13.0 (0.0e25.0) 0.4 % Intervention history: 51.0 (35.0e68.0) 74.0 (58.0e91.0) 0.08 Urethroplasty 5.0 (0.0e12.0) 3.0 (0.0e10.0) 0.59 Hypospadias 10.0 (0e20.0) 3.0 (0.0e10.0) 0.37 % Stricture etiology: Iatrogenic 33.0 (18.0e49.0) 29.0 (12.0e46.0) 0.8 Idiopathic 67.0 (51.0e82.0) 71.0 (54.0e88.0) 0.8 % Repair: EPA 72.0 (57.0e87.0) 74.0 (58.0e91.0) 1 Dorsal onlay þ graft 28.0 (13.0e43.0) 23.0 (7.0e38.0) 0.78 Ventral onlay þ graft (0.0e10.0) 0.44 % Postop complication (0.0e16.0) 0.19 % Recurrent stricture requiring repeat procedure 3.0 (0.0e8.0) 16.0 (2.0e30.0) 0.08 * Mann-Whitney U and Fisher exact tests. urologist elsewhere. In patients without recurrence at last followup the incidence of LS on re-review was 40.6% (95% CI 28.3e52.3) vs 83.3% (95% CI 40.5e100) in patients with recurrence. Recurrence was significantly more common in patients with pathology findings suggestive of or diagnostic for LS (p ¼ 0.04). DISCUSSION To our knowledge the true incidence of male urethral LS is unknown. However, several retrospective studies estimated that incidence of LS in males undergoing evaluation or repair of urethral strictures was 4.8% to 29%. 3,14 In a retrospective study of 1,439 men with urethral stricture Palminteri et al reported LS as the etiology of stricture in 13.5% overall with specific involvement of the penile urethra in 24.4%, penile plus bulbar urethra in 23.9% and panurethral involvement in 48.6%. 3 Notably no patient was identified with LS in an isolated bulbar stricture or posterior stenosis. Barbagli reviewed the records of 106 patients treated with urethroplasty for anterior urethral stricture, including 29% with a pathological diagnosis of LS. 8 LS involved the meatus in 19% of patients, fossa navicularis in 17%, penile urethra in 3% and the entire urethra in 52%. Similar to the study by Palminteri et al, 3 there was no mention of an isolated bulbar stricture associated with LS. 8 Other
4 778 LICHEN SCLEROSUS AND ISOLATED BULBAR URETHRAL STRICTURE DISEASE reports of the etiopathogenesis of LS in urethral stricture corroborate these findings. 7,15,16 In our study 70 men underwent urethroplasty for isolated bulbar urethral stricture. Notably pathology evaluation at surgery revealed evidence of LS in 7.1% of these patients. On histopathological re-review by a blinded uropathologist using an expert, consensus driven rubric of characteristic pathological findings for LS 44.3% of men had pathological findings consistent with LS, which were suggestive in 18.6% and diagnostic in 25.7%. The statistically significant increase in LS identified on re-review suggests that a combination of evaluation by a specialized uropathologist and reference to characteristic histopathological findings of LS may allow for a higher detection rate. As a result of rigorous reexamination of isolated bulbar urethral stricture specimens at our institution, 26 cases of previously unrecognized LS were identified. To our knowledge this report represents the only series in which LS was identified pathologically after urethroplasty in isolated bulbar urethral strictures with no evidence of progressive disease extending to the bulbar urethra from more distal disease. Despite the study limitations these data call into question previously accepted beliefs regarding the pathogenesis and pathophysiology of LS distal to proximal progression patterns in the male urethra. While the described incidence of LS may be higher than in the general population due to selection bias at a tertiary referral center, identification of any LS in isolated bulbar urethral strictures is a novel finding that questions the existing understanding of the pathophysiology of disease progression. We diagnosed LS on re-review according to a newly developed histopathological evaluation system based on 5 tissue features, including hyperkeratosis, thinning or thickening of the epidermis or squamous epithelium, attenuation or vacuolar degeneration of the basal cell layer, subepithelial hyalinization/dermal collagen homogenization and lichenoid lymphocytic or plasmacytic infiltrate. 13 It is intriguing that almost half of our patients with isolated bulbar stricture had at least 2 of these features. This could suggest that such features of mucosal atrophy are the result of an aberrant healing process and LS may become fully apparent at the end of this process. Therefore, LS could be seen as a symptom of aberrant wound healing resulting in mucosal atrophy rather than as a disease process. Further studies of these histopathological features in separate patient cohorts with isolated bulbar urethral stricture specimens would contribute to answering this question. LS has long been associated with stricture disease chronicity with a subsequent increased risk of recurrence despite aggressive surgical management. 8 Recurrence developed in 6 of our 70 study patients (8.6%) during the median followup of 22 months. Five of the 6 patients (83.3%) with recurrence had LS on pathology re-review. Notably mean stricture length in those with and without stricture recurrence did not statistically differ (3.5 and 4.3 cm, respectively). Pathological evidence of LS on re-review was significantly associated with recurrence (p ¼ 0.04). These results support existing literature on the increased risk of recurrence in patients with LS after definitive surgical management. 8 Stricture recurrence is likely multifactorial, involving patient comorbidity, surgical technique and surgical factors not captured in this study. LS may still exist in other areas of the urethra that are not sampled at urethroplasty despite focal bulbar stricture disease. Thus, our findings may result from a 2-part scenario in which LS and another insult to the bulbar urethra may translate to clinically significant stricture. Nonetheless, preoperative suspicion for LS involvement in isolated bulbar stricture segments may alter the management strategy through the reconstructive approach offered, namely EPA vs substitution urethroplasty. The diagnosis of LS involvement in a short, isolated bulbar urethral stricture would also influence patient counseling on endoscopic approaches to establish urethral patency due to the aggressive pathophysiology of LS. Although our study is limited by its retrospective, single institution nature and limited sample size, we believe that our findings remain significant and warrant further investigation in regard to LS pathophysiology. Previously unrecognized LS was detected in isolated bulbar stricture segments in a significant proportion of our study cohort of 70 patients. We think that these results require elaboration and confirmation in a large multi-institutional cohort with multiple pathologists. Our study is also limited by followup duration, which may have prevented the recognition of certain patient variables associated with recurrence after urethroplasty that were not identified. Controversy exists regarding optimal management of urethral LS with some groups proposing complete excision of the involved urethral mucosa and repair with 1-stage or staged urethroplasty using a nongenital skin graft 7,17,18 while others suggest consideration of perineal urethrostomy, particularly in the elderly population. 19 Identifying LS before or at surgery may enable identification of stricture etiology and also provide guidance for surgical management as well as a long-term followup strategy for stricture recurrence and potential malignancy risk related to LS.
5 LICHEN SCLEROSUS AND ISOLATED BULBAR URETHRAL STRICTURE DISEASE 779 CONCLUSIONS We report a significant incidence of LS in isolated bulbar urethral stricture disease in men treated with urethroplasty on re-review of surgical specimens. To our knowledge this has not been reported previously. The incidence of LS may be higher than previously believed in isolated bulbar urethral stricture segments. Early recognition of LS in an isolated bulbar urethral stricture may influence treatment planning and followup. REFERENCES 1. Powell JJ and Wojnarowska F: Lichen sclerosus. Lancet 1999; 353: Philippou P, Shabbir M, Ralph DJ et al: Genital lichen sclerosus/balanitis xerotica obliterans in men with penile carcinoma: a critical analysis. BJU Int 2013; 111: Palminteri E, Berdondini E, Verze P et al: Contemporary urethral stricture characteristics in the developed world. Urology 2013; 81: Dubey D, Sehgal A, Srivastava A et al: Buccal mucosal urethroplasty for balanitis xerotica obliterans related urethral strictures: the outcome of 1 and 2-stage techniques. J Urol 2005; 173: Mangera A and Chapple C: Management of anterior urethral stricture: an evidence-based approach. Curr Opin Urol 2010; 20: Meeks JJ, Barbagli G, Mehdiratta N et al: Distal urethroplasty for isolated fossa navicularis and meatal strictures. BJU Int 2012; 109: 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: Barbagli G, Lazzeri M, Palminteri E et al: Lichen sclerosis of male genitalia involving anterior urethra. Lancet 1999; 354: Barbagli G, Mirri F, Gallucci M et al: Histological evidence of urethral involvement in male patients with genital lichen sclerosus: a preliminary report. J Urol 2011; 185: Barbagli G, Palminteri E, Balo S et al: Lichen sclerosus of the male genitalia and urethral stricture diseases. Urol Int 2004; 73: Clouston D, Hall A and Lawrentschuk N: Penile lichen sclerosus (balanitis xerotica obliterans). BJU Int 2011; 108: Murphy R: Lichen sclerosus. Dermatol Clin 2010; 28: Prabhu SV, Liu JS, Gonzalez CM et al: Lichen sclerosus, a common finding in urethral strictures in males. Mod Pathol, suppl., 2013; 27: 253A. 14. Stein DM, Thum DJ, Barbagli G et al: A geographic analysis of male urethral stricture aetiology and location. BJU Int 2013; 112: Depasquale I, Park AJ and Bracka A: The treatment of balanitis xerotica obliterans. BJU Int 2000; 86: Lumen N, Hoebeke P, Willemsen P et al: Etiology of urethral stricture disease in the 21st century. J Urol 2009; 182: Pugliese JM, Morey AF and Peterson AC: Lichen sclerosus: review of the literature and current recommendations for management. J Urol 2007; 178: Levine LA, Strom KH and Lux MM: Buccal mucosa graft urethroplasty for anterior urethral stricture repair: evaluation of the impact of stricture location and lichen sclerosus on surgical outcome. J Urol 2007; 178: Peterson AC, Palminteri E, Lazzeri M et al: Heroic measures may not always be justified in extensive urethral stricture due to lichen sclerosus (balanitis xerotica obliterans). Urology 2004; 64: 565.
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