Original Article Clinical, Trichoscopic, and Histopathological Features of Primary Access this article online Website: Cicatricial Alopecias: A Retrospective www.ijtrichology.com Observational Study at a Tertiary Care DOI: Centre of North East India 10.4103/0974-7753.167459 Quick Response Code: Binod Kumar Thakur, Shikha Verma, Vandana Raphael1

Departments of Dermatology and STD and 1Pathology, North Eastern Indira Gandhi Regional Institute of Health and Medical Sciences, Shillong, Meghalaya, India

ABSTRACT

Background: The primary cicatricial alopecias (PCAs) are a rare group of diseases where hair follicle is the primary target of destruction. There are a few studies on histopathological and trichoscopic features of PCA. Aims: To study the clinical, trichoscopic, and histopathological characteristics of PCAs of the scalp and to find out the concordance between trichoscopic and histopathological diagnosis. Materials and Methods: We retrospectively analyzed the clinical, trichoscopic, and histopathological features of 24 PCA patients. Fisher’s Chi‑square exact test was done to find the significant trichoscopic and histopathological features. Cohen’s kappa coefficient was used to determine the agreement between histopathological and trichoscopic diagnosis. Results: A total of 24 patients of PCA were seen with a male: female ratio of 2:1. There were 10 (41.7%) patients of discoid lupus erythematosus (DLE), 5 (20.8%) of lichen planopilaris (LPP), 3 (12.5%) of dissecting cellulitis of scalp, and 2 (8.3%) each of pseudopelade of brocq, decalvans, and frontal fibrosing alopecia. The important histopathological findings of DLE were follicular plugging, vacuolar changes in the basal layer, necrotic keratinocytes, and superficial and deep perifollicular and perivascular lymphocytic infiltrate. Histopathology of LPP showed vacuolar changes in the basal layer Address for correspondence: and lichenoid infiltrate involving the infundibulum and isthmus. Trichoscopy of DLE showed Dr. Binod Kumar Thakur, follicular plugging, yellow dots, and thick arborizing blood vessels. The peripilar cast was Department of Dermatology important finding in LPP. The characteristic yellow dot with three‑dimensional structure and STD, North Eastern Indira was noted in dissecting cellulitis of the scalp. The Cohen’s kappa agreement was 0.89 Gandhi Regional Institute of between histopathological and trichoscopic diagnosis. Conclusion: The diagnosis of PCA Health and Medical Sciences, is challenging because of overlapping features clinically and histopathologically. Trichoscopy may provide quick and reliable diagnosis and obviate the necessity of scalp biopsy in busy Mawdiangdiang ‑ 793 018, clinics. Shillong, Meghalaya, India. E‑mail: binod.k.thakur@ gmail.com Key words: Histopathology, primary cicatricial alopecia, trichoscopy

INTRODUCTION characteristic features and aids to the diagnosis. The aim of the present study was to retrospectively analyze the rimary cicatricial alopecia (PCA) is an uncommon clinical, trichoscopic, and histopathological characteristics Pand clinically diverse set of disorders in which the of PCA of the scalp and to find out the concordance hair follicle is irreversibly destroyed leading to permanent This is an open access article distributed under the terms of the Creative alopecia. In 2001, North American Hair Research Society, Commons Attribution‑NonCommercial‑ShareAlike 3.0 License, which allows issued a consensus opinion on classification of the PCA others to remix, tweak, and build upon the work non‑commercially, as long as the author is credited and the new creations are licensed under the identical terms. based on principal inflammatory cell type in a representative biopsy sample from the scalp.[1] For reprints contact: [email protected] How to cite this article: Thakur BK, Verma S, Raphael V. Clinical, The diagnosis of PCA is challenging because of trichoscopic, and histopathological features of primary cicatricial overlapping features both clinically and histopathologically. alopecias: A retrospective observational study at a tertiary care Trichoscopy is a noninvasive procedure which shows centre of North East India. Int J Trichol 2015;7:107-12.

© 2015 International Journal of Trichology | Published by Wolters Kluwer - Medknow 107 Thakur, et al.: Clinical, trichoscopic, and histopathological features of primary cicatricial alopecias between trichoscopic and histopathological diagnosis Table 1: Summary of clinical features of primary in PCA. cicatricial alopecia Cases Sex (%) Age (years) n=24 (%) Male, Female, Mean Range MATERIALS AND METHODS n=16 n=8 DLE 10 (41.7) 6 (37.5) 4 (50.0) 28.7 3-76 All the patients of PCA who attended Dermatology LPP 5 (20.8) 3 (18.8) 2 (25.0) 29.2 23-36 Outpatient Department from April 2013 to September 2014 Pseudopelede of Brocq 2 (8.3) 2 (12.5) - 25 21-29 were included in the present study. We retrospectively Dissecting cellulitis of scalp 3 (12.5) 3 (18.8) - 16 14-18 analyzed the clinical data, trichoscopic, and histopathological 2 (8.3) 2 (12.5) - 22 16-28 features of 24 patients of PCA. The diagnosis was Frontal fibrosing alopecia 2 (8.3) - 2 (25.0) 61 60-62 confirmed on the basis of clinical, histopathological, LPP – Lichen planopilaris; DLE – Discoid lupus erythematosus and trichoscopic features. The age, sex, duration, clinical findings, concomitant diseases, and other relevant history scalp in males. There were multiple, erythematous, were recorded. The blood tests like complete blood count, scaly, atrophic, hypopigmented patches with peripheral blood sugar, liver and kidney function, and antinuclear hyperpigmentation. In 4 (40%) patients, the lesions were also antibody were performed in relevant cases. The trichoscopy present on other body areas. In 3 (30%) cases, scalp DLE was performed with a digital dermoscope and the images was associated with systemic lupus erythematosus. saved. Punch biopsy of 4 mm was taken from the active margin of alopecia patches, and in most cases vertical Lichen planopilaris sectioning was done. The slides were stained with eosin The involvement in all patients was on the frontoparietal and hematoxylin and studied under microscope. Pus for scalp. Violaceous patches of scarring alopecia with culture and sensitivity was done in relevant patients. The perifollicular scaling were seen. Itching was an important study was approved by Institutional Ethics Committee. symptom in all the patients. None had lesions on the mouth or other body sites. Statistical analysis Frontal fibrosing alopecia The collected data were analyzed using SPSS version 22 (IBM SPSS Statistics, Version 22.0. Armonk, NY: IBM Corp.). Two postmenopausal females presented with band like Fisher’s Chi‑square exact test was performed for intergroup progressive scarring alopecia of the frontal scalp. The hairs on comparisons. A P < 0.05 were considered statistically the active margin showed perifollicular scaling. There was no significant. The agreement between histopathological involvement of eyebrows. However, pigmentosus diagnosis and trichoscopic diagnosis was calculated using lesion was present on other body areas in one of the patients. Cohen’s kappa coefficient. Pseudopelade of brocq

RESULTS There were multiple skin colored atrophic patches of scarring alopecia of variable sizes. There was no history Clinical features of any on the affected area. One patient had associated scalp psoriasis. There were 24 patients of PCA, with a male: female ratio of 2:1. The age group ranged from 3 to 76 years. Dissecting cellulitis of scalp The study comprised of 10 cases of discoid lupus erythematosus (DLE), five cases of lichen planopilaris (LPP), All patients had multiple, painful, pustules, nodules, and three cases of dissecting cellulitis of scalp, two cases each abscesses with areas of scarring alopecia on the scalp. Pus of pseudopelade of brocq, folliculitis decalvans, and frontal for culture and sensitivity was sterile. All had associated fibrosing alopecia (FFA) [Figures 1‑6]. The various clinical moderate vulgaris. features are summarized in Table 1. Folliculitis decalvans Discoid lupus erythematosus Two patients had recurrent follicular pustules on the scalp The patients include six males and four females. The most with areas of scarring alopecia on the previously affected common site was occipital scalp in females and frontoparietal site. Follicular tufting was not seen in our patients.

108 International Journal of Trichology / Jul-Sep 2015 / Vol-7 / Issue-3 Thakur, et al.: Clinical, trichoscopic, and histopathological features of primary cicatricial alopecias

a b a b

c d c d Figure 1: Discoid lupus erythematosus (a) clinical (b) histopathology Figure 2: Lichen planopilaris (a) clinical (b) histopathology H and E, ×40 (c and d) dermoscopic findings H and E, ×40 (c and d) dermoscopic findings

a b a b

c d c d Figure 3: Frontal fibrosing alopecia (a) clinical (b) histopathology Figure 4: Pseudopelade of brocq (a) clinical (b) histopathology H and E, ×40 (c and d) dermoscopic findings H and E, ×40 (c and d) dermoscopic findings

a b a b

c d c d Figure 5: Dissecting cellulitis of scalp (a) clinical (b) histopathology Figure 6: Folliculitis decalvans (a) clinical (b) histopathology H and E, ×100 (c and d) dermoscopic findings H and E, ×100 (c and d) dermoscopic findings

Trichoscopic features atrophy in all the patients. Scattered brownish discoloration was seen in 70% DLE patients while thick arborizing blood Trichoscopy showed absent follicular opening and epidermal vessels were seen in 80% cases of DLE. The peripilar cast International Journal of Trichology / Jul-Sep 2015 / Vol-7 / Issue-3 109 Thakur, et al.: Clinical, trichoscopic, and histopathological features of primary cicatricial alopecias was seen in 100% patients of LPP. Scattered single hair perfect agreement (kappa coefficient = 0.89) between follicles were noted in FFA. Follicular pustules were seen histological and trichoscopic diagnosis. in folliculitis decalvans. A three‑dimensional (3D) yellowish structure was specifically seen in all patients of dissecting cellulitis of the scalp. The various trichoscopic features are DISCUSSION shown in Table 2. In PCA, the inflammatory process is folliculocentric [2] Histopathological features with the hair follicle as the main target. The destruction of epithelial stem cells in the bulge of the outer Hair follicles were replaced by fibrous connective tissue with root sheath prevents the regeneration of hair.[3,4] In a variable degree in all the patients. The sebaceous glands a retrospective study by Whiting, cicatricial alopecia were either decreased or absent. Interface changes were was diagnosed in 7.3% (n = 427) of all patients who noted in both LPP (100%) and DLE (90%). In LPP, the underwent an evaluation over a 10‑year period.[5] In two perifollicular lymphocytic infiltrate was mostly seen in the 5‑year retrospective studies by Tan et al. and Qi et al., superficial dermis. However, in DLE, the infiltrate was both PCA was reported in 3.2% (n = 112) and 2.1% (n = 59) perifollicular and perivascular, and located in both superficial of the patients, respectively.[2,6] Whiting observed and deep dermis. Mucin deposition was noted only in DLE. pseudopelade predominantly (40.6%), followed by Neutrophilic abscesses were seen in both folliculitis decalvans LPP (12.6%) and folliculitis decalvans (11.2%).[5] Tan et al. and dissecting cellulitis of the scalp. Granuloma with foreign reported DLE as the most common (33.9%), followed body giant cells was seen in both cases of dissecting cellulitis by pseudopelade (24.1%) and LPP (22.3%).[2] Trachsler of the scalp. Minor inflammation was evident in pseudopelade and Trueb studied 136 biopsy specimens of scarring of brocq. The salient histopathological features observed are alopecia and found that the most frequent diagnosis summarized in Table 3. was LPP (26%), followed by DLE (21%), folliculitis decalvans (20%), and pseudopelade of Brocq (10%).[7] The diagnosis of PCA based on trichoscopic feature and In these studies, most of the cases were lymphocytic but histopathological features was compared. There was a one study from China reported folliculitis decalvans as the

Table 2: Trichoscopic features of various types of primary scarring alopecias Trichoscopic features DLE LPP Frontal fibrosing Pseudopelade Dissecting Folliculitis P (n=10) (%) (n=5) (%) alopecia of Brocq cellulitis of decalvans (n=2) (%) (n=2) (%) scalp (n=3) (%) (n=2) (%) Follicular features Yellow dots 7 (70) - - 1 (50) 2 (66.67) - 0.031# Black dots 2 (20) - - - 2 (66.67) 2 (100) 0.044# 3D yellow dots - - - - 3 (100) - <0.001# Classic white dots - - 1 (50) - - - 0.25 Absent follicular openings 10 (100) 5 (100) 2 (100) 2 (100) 3 (100) 2 (100) - Follicular pustules - - - - 2 (66.67) 2 (100) 0.002# Follicular hyperkeratosis 9 (90) - 1 (50) - 1 (33.33) - 0.001# Peripilar casts - 5 (100) 2 (100) - 1 (33.33) - <0.001# Predominance of one hair follicles - - 2 (100) - - - 0.011# Perifollicular and interfollicular features Thick arborizing blood vessels 8 (80) - - - - - 0.002# Elongated linear blood vessels - 2 (40) 2 (100) - 1 (33.33) 2 (100) 0.003# Scattered brown discoloration of the scalp skin 7 (70) 2 (40) 1 (50) - - - 0.128 Perifollicular erythema 10 (100) 3 (60) 2 (100) - 2 (66.67) 2 (100) 0.023# Perifollicular scaling 8 (80) 5 (100) 1 (50) - 2 (66.67) - 0.020# Interfollicular scaling 10 (100) 1 (20) 1 (50) - 1 (33.33) - <0.001# Epidermal atrophy 10 (100) 5 (100) 2 (100) 2 (100) 3 (100) 2 (100) - Cicatricial white patches 10 (100) 5 (100) 2 (100) 2 (100) 3 (100) 2 (100) - Blue grey dots 2 (20) - 1 (50) - - - 0.491 Yellow crusts - - - - 3 (100) - <0.001#

#P<0.05. LPP – Lichen planopilaris; DLE – Discoid lupus erythematosus

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Table 3: Histopathological features of various types of primary cicatricial alopecias DLE LPP Frontal Pseudopelede Dissecting Folliculitis P (n=9) (%) (n=6) (%) fibrosing of Brocq (n=2) cellulitis decalvans alopecia (%) of scalp (n=3) (%) (n=2) (%) (n=2) (%) Hair follicle perifollicular lymphocytes 9 (100) 6 (100) 2 (100) 1 (50) - - <0.001# Hair follicle perifollicular neutrophils and neutrophilic abscesses - - - - 2 (100) 3 (100) <0.001# Vacuolar changes in basal layer 9 (100) 5 (83.33) 2 (100) - 1 (50) - <0.001# Necrotic keratinocytes 6 (66.67) 2 (33.33) - - 1 (50) - 0.201 Orthokeratosis 6 (66.67) 3 (50) 1 (50) - - - 0.207 Parakeratosis 4 (44.44) - - - 1 (50) 3 (100) 0.023# Follicular plugging 8 (88.88) 4 (66.67) 2 (100) 1 (50) 2 (100) 3 (100) 0.589 Involvement of inter follicular epidermis 8 (88.88) 3 (50) 2 (100) 2 (100) 2 (100) 3 (100) 0.367 Perifollicular fibrosis 6 (66.67) 3 (50) - 2 (100) - - 0.075 Polytrichia - - - - - 1 (33.33) 0.375 Granuloma formation - - - - 2 (100) - 0.011#

#P<0.05. LPP – Lichen planopilaris; DLE – Discoid lupus erythematosus most common (40%).[6] The different clinical presentations arborizing vessels and large yellow dots.[14] Scattered brown could be because of ethnic and demographic variations. discoloration may be seen in some patients.[14] In our patients, thick arborizing vessels were seen only in 80% There are very few studies on cicatricial alopecia from cases. Red dots are considered a good prognostic factor India,[8,9] and to our knowledge, this is the first report of hair regrowth.[15] It was reported in 25% and 38% DLE of trichoscopic as well as the histopathological study of cases in previous studies.[6,15] The red dots were not seen PCA from India. In both the Indian studies, DLE was in our patients. This may be due to brown skin color of the most common cause of PCA reported in 79.16% and our patients. The trichoscopic and pathologic features of 49% cases, respectively. In our study also, DLE was the FFA and LPP are identical and include absence of follicular most common, seen in 41.7% cases. Dissecting cellulitis openings, cicatricial white patches, peripilar casts, blue‑gray of the scalp (12.5%) and FFA (8.3%) were not observed in dots, and perifollicular erythema.[16] previously reported Indian studies. Traditionally, the criteria for diagnosis of DLE in histopathology are epidermal In FFA, the hair follicles are of single hair follicular units. atrophy, interface dermatitis, superficial and deep dermal The most characteristic trichoscopic feature of classic LPP lymphocytic inflammation, periadnexal inflammation, is white perifollicular scaling and scales entangling hair papillary dermal fibrosis, dermal mucin, and thickened shafts up to 2–3 mm above scalp surface.[14] Peripilar casts periodic acid‑Schiff‑positive epidermal and follicular were also seen in all cases of LPP and FFA. Folliculitis basement membrane.[10] These criteria were observed decalvans is characterized by the presence of multiple in most of our cases. The classic histological features hairs in one follicular unit.[17] Tufted hairs were not seen in described in LPP are the presence of a lichenoid interface our patients. It was seen in 12.5% cases in a recent study.[6] dermatitis of the upper portions of the follicle.[10,11] The The finding of tufted hair may be related to the severity inflammation in LPP is mostly lymphocytic with preferential of folliculitis decalvans.[18] A specific finding in dissecting involvement of the peri‑infundibular and isthmic regions. cellulitis of the scalp is yellow dots with 3D structure The superficial and deep perifollicular and perivascular imposed over a thick, black, hair shaft residue.[19] We noted lymphocytic infiltrate, the presence of abundant dermal this finding in all cases of dissecting cellulitis of the scalp. melanophages in DLE helped to differentiate with LPP Trichoscopic features of classic pseudopelade of Brocq are in our cases. nonspecific. Thus, pseudopelade of Brocq is a diagnosis of exclusion both clinically and trichoscopically.[20,21] Trichoscopy (dermoscopic examination of scalp and hair) is a very useful technique for the diagnosis and follow‑up There was 89% concordance between trichoscopic and of hair and scalp disorders.[12,13] Trichoscopy of primary histopathological diagnosis in our study. A limitation of scarring alopecia is characterized by decreased hair density this study is retrospective design and a small number of and loss of follicular openings. The most characteristic patients in each type of PCA. As there is too much overlap trichoscopic features of DLE of the scalp are thick in the histopathological features of folliculitis decalvans

International Journal of Trichology / Jul-Sep 2015 / Vol-7 / Issue-3 111 Thakur, et al.: Clinical, trichoscopic, and histopathological features of primary cicatricial alopecias and dissecting cellulitis of the scalp, clinicopathological 6. Qi S, Zhao Y, Zhang X, Li S, Cao H, Zhang X. Clinical features of primary cicatricial alopecia in Chinese patients. Indian J Dermatol Venereol Leprol correlation and trichoscopic evaluation of neutrophilic 2014;80:306‑12. variants of PCA help in proper diagnosis. We suggest that 7. Trachsler S, Trueb RM. Value of direct immunofluorescence for differential for proper diagnosis of PCA, both histopathology and diagnosis of cicatricial alopecia. Dermatology 2005;211:98‑102. trichoscopy are essential and for follow‑up trichoscopy 8. Kumar UM, Yelikar BR. The spectrum of histopathological lesions in scarring alopecia: A prospective study. J Clin Diagn Res 2013;7:1372‑6. is very helpful. However, trichoscopy may provide quick 9. Inchara YK, Tirumalae R, Kavdia R, Antony M. Histopathology of scarring and reliable diagnosis and obviate the necessity of scalp alopecia in Indian patients. Am J Dermatopathol 2011;33:461‑7. biopsy in a busy clinic. 10. Sperling LC, Cowper SE. The histopathology of primary cicatricial alopecia. Semin Cutan Med Surg 2006;25:41‑50. 11. Tandon YK, Somani N, Cevasco NC, Bergfeld WF. A histologic review of Financial support and sponsorship 27 patients with lichen planopilaris. J Am Acad Dermatol 2008;59:91‑8. 12. Olszewska M, Rudnicka L, Rakowska A, Kowalska‑Oledzka E, Slowinska M. Nil. Trichoscopy. Arch Dermatol 2008;144:1007. 13. Jain N, Doshi B, Khopkar U. Trichoscopy in alopecias: Diagnosis simplified. Conflicts of interest Int J Trichology 2013;5:170‑8. 14. Rakowska A, Slowinska M, Kowalska‑Oledzka E, Warszawik O, Czuwara J, Olszewska M, et al. Trichoscopy of cicatricial alopecia. J Drugs Dermatol There are no conflicts of interest. 2012;11:753‑8. 15. Tosti A, Torres F, Misciali C, Vincenzi C, Starace M, Miteva M, et al. Follicular red dots: A novel dermoscopic pattern observed in scalp discoid lupus REFERENCES erythematosus. Arch Dermatol 2009;145:1406‑9. 16. Duque‑Estrada B, Tamler C, Sodré CT, Barcaui CB, Pereira FB. Dermoscopy 1. Olsen EA, Bergfeld WF, Cotsarelis G, Price VH, Shapiro J, Sinclair R, et al. patterns of cicatricial alopecia resulting from discoid lupus erythematosus Summary of North American Hair Research Society (NAHRS)‑sponsored and lichen planopilaris. An Bras Dermatol 2010;85:179‑83. Workshop on Cicatricial Alopecia, Duke University Medical Center, 17. Otberg N, Kang H, Alzolibani AA, Shapiro J. Folliculitis decalvans. Dermatol February 10 and 11, 2001. J Am Acad Dermatol 2003;48:103‑10. Ther 2008;21:238‑44. 2. Tan E, Martinka M, Ball N, Shapiro J. Primary cicatricial alopecias: 18. Sillani C, Bin Z, Ying Z, Zeming C, Jian Y, Xingqi Z. Effective treatment Clinicopathology of 112 cases. J Am Acad Dermatol 2004;50:25‑32. of folliculitis decalvans using selected antimicrobial agents. Int J Trichology 3. Harries MJ, Paus R. The pathogenesis of primary cicatricial alopecias. 2010;2:20‑3. Am J Pathol 2010;177:2152‑62. 19. Rudnicka L, Rakowska A, Olszewska M. Trichoscopy: How it may help the 4. Harries MJ, Trueb RM, Tosti A, Messenger AG, Chaudhry I, Whiting DA, et al. clinician. Dermatol Clin 2013;31:29‑41. How not to get scar (r) ed: Pointers to the correct diagnosis in patients with 20. Rudnicka L, Olszewska M, Rakowska A, editors. Trichoscopy: Dermoscopy suspected primary cicatricial alopecia. Br J Dermatol 2009;160:482‑501. of hair and scalp. London: Springer‑Verlag; 2012. 5. Whiting DA. Cicatricial alopecia: Clinico‑pathological findings and 21. Alzolibani AA, Kang H, Otberg N, Shapiro J. Pseudopelade of brocq. treatment. Clin Dermatol 2001;19:211‑25. Dermatol Ther 2008;21:257‑63.

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