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E-IJD® - ORIGINAL ARTICLE |
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| Year : 2022 | Volume
: 67
| Issue : 5 | Page : 624 |
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| Clinico-epidemiology and histopathologic spectrum of primary scarring alopecia: A cross-sectional study |
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Souvik Sardar1, Somenath Sarkar2, Indrashis Podder3, Gautam Banerjee4
1 Dermatologist, Eleganz Skin and Hair Clinic, Kolkata, West Bengal, India
2 Department of Dermatology, Bankura Sammilani Medical College and Hospital, Bankura, West Bengal, India
3 Department of Dermatology, College of Medicine and Sagore Dutta Hospital, Kolkata, West Bengal, India
4 Department of Dermatology, School of Tropical Medicine, Kolkata, West Bengal, India
| Date of Web Publication | 29-Dec-2022 |
Correspondence Address:
Indrashis Podder
College of Medicine and Sagore Dutta Hospital, Kamarhati, Kolkata - 700 058, West Bengal
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/ijd.ijd_540_21
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 Abstract | | |
Background: Primary scarring alopecias (PSAs) are a rare group of dermatological disorders with overlapping clinical features. They result in permanent hair loss and significant psychological morbidity. Aims: To analyze the clinico-epidemiology of PSAs of the scalp, along with clinico-pathological correlation. Methods: We conducted a cross sectional, observational study including 53 histopathologically confirmed cases of PSA. Clinico-demographic parameters, hair care practices, and histologic characteristics were noted and statistically analyzed. Results: Among 53 patients (mean age 30.9 ± 8.1 years, M: F 1:1.2, median duration 4 years) with PSA, lichen planopilaris (LPP) was most common (39.6%, 21/53), followed by pseudopelade of Brocq [30.2%, 16/53], discoid lupus erythematosus (DLE) [16.9%, 9/53], and non-specific scarring alopecia (SA) (7.5%, 4/53), while central centrifugal cicatricial alopecia (CCCA), folliculitis decalvans, and acne keloidalis nuchae (AKN) accounted for 1 case each. Forty-seven patients (88.7%) demonstrated predominant lymphocytic inflammatory infiltrate, while basal cell degeneration and follicular plugging were the commonest histological changes. Perifollicular erythema and dermal mucin deposition were noted in all patients with DLE (both P < 0.05). Nail involvement (P = 0.004) and mucosal involvement (P = 0.8) were more common in LPP. Single alopecic patches were characteristic of DLE and CCCA. Hair care practices (non-medicated shampoo > oil) had no significant association with the subtype of PSA. (P = 0.4) Conclusion: PSAs are a diagnostic challenge for dermatologists. Thus, histology and clinico-pathological correlation should be performed in all cases for proper diagnosis and treatment.
Keywords: Hair loss, histology, primary scarring alopecia, scalp
How to cite this article:
Sardar S, Sarkar S, Podder I, Banerjee G. Clinico-epidemiology and histopathologic spectrum of primary scarring alopecia: A cross-sectional study. Indian J Dermatol 2022;67:624 |
How to cite this URL:
Sardar S, Sarkar S, Podder I, Banerjee G. Clinico-epidemiology and histopathologic spectrum of primary scarring alopecia: A cross-sectional study. Indian J Dermatol [serial online] 2022 [cited 2023 Jun 7];67:624. Available from: https://www.e-ijd.org/text.asp?2022/67/5/624/366135 |
| Introduction | |  |
Scarring alopecia (SA) or cicatricial alopecia refers to a heterogeneous group of cutaneous disorders characterized by permanent hair loss, due to irreversible destruction of hair follicles and their epithelial stem cells.[1] The hair loss results in an unsightly physical appearance, thus leading to significant psychological morbidity and poor quality of life.[2]
SAs can be further subdivided as primary scarring alopecia (PSA) and secondary scarring alopecia (SSA). PSA includes a rare, diverse group of disorders characterized by irreversible destruction of hair follicles resulting in scarring and permanent hair loss. This is clinically manifested by lack of follicular ostia, while the histological hallmark is the replacement of hair follicle structures by reparative fibrous tissue. In SSA, the destruction of hair follicle is not the primary pathology, rather it occurs as a result of exogenous insults like trauma (e.g., burns, radiation, traction), infections (e.g., tinea capitis, herpes virus infections), or endogenous immunological and inflammatory disorders like sarcoidosis, morphea/scleroderma, and pemphigus or tumors.[1],[2] Recently, inflammatory bowel disease and serum Vitamin D deficiency have been proposed as possible risk factors for developing PSA.[1],[3]
Although several classifications exist for PSA, the North American Hair Research society (NAHRS) classification is accepted most widely.[4] This system subdivided PSA into four groups based on predominant inflammatory infiltrates and included relevant clinical entities in each group—lymphocytic group [e.g., chronic cutaneous lupus erythematosus (CCLE), lichen plano pilaris (LPP) and its variants, pseudopelade of Brocq (PPB) and central centrifugal cicatricial alopecia (CCCA)], neutrophilic group [folliculitis decalvans (FD) and dissecting cellulitis of the scalp (DC)], mixed group [acne keloidalis nuchae (AKN)], and non-specific group. [Table 1]. | Table 1: Classification of primary scarring (cicatricial) alopecia by NAHRS [4]
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PSA are a diagnostic challenge due to overlapping clinical and histopathological features, more so in cases of delayed presentation due to non-specific histology. The rarity of this disease has resulted in limited published work about this condition from India, especially in the present setup. Thus, we undertook this study to analyze the clinico-epidemiological profile of SA in our setup, along with their histopathological features and clinico-pathological correlation.
| Materials and Methods | | |
Study population
We included all patients with PSA attending our outpatient department (OPD) during the study period (January to December 2019; 12 months), irrespective of age and gender. Clinically, SA was diagnosed as an area of hair loss without visible follicular ostia. Diagnoses of SSA (e.g., tumors, infections, trauma, inflammatory disorders, and tumors), progression of hair loss beyond the scalp, immunosuppression due to systemic disorders like DM or systemic medications (due to risk of delayed healing post-biopsy), known bleeding disorders, low platelet count, increased bleeding or clotting time, presence of active dermatitis/infection supervening the biopsy site and refusal for skin biopsy comprised our exclusion criteria. Finally, we enrolled 53 study subjects with histologically confirmed PSA after fulfilling the inclusion and exclusion criteria.
Study design
We conducted a cross section, observational study at a tertiary care center, Eastern India over a period of 12 months. The study was approved by the institutional ethics committee and conducted in strict accordance with the ethical principles of the modified Declaration of Helsinki 1964, the International Conference on Harmonization principles of Good Clinical Practice. After screening for eligibility, each patient was subjected to detailed history taking including demographic parameters, duration of disease, mode of onset, clinical features, any hair care practice, (non-medicated shampoo, hair oil, hair color, and physical modalities like hair straightening or hair braiding) and concomitant disease. We performed a detailed dermatological examination to assess the site of hair loss by dividing the scalp into five anatomical regions—frontal, parietal, vertex, temporal, and occipital; clinical signs (scaling/perifollicular erythema/papule or pustule) and pattern of clinical presentation—follicular/non-follicular, single/multiple alopecic patches, borders (regular/irregular) and size [small (≤3 cm) or large (>3 cm)]. The clinical pattern was categorized into five types such as follicular, multiple-regular, multiple-irregular, single-small, and single-large. Additionally, nails, mucosae, skin, and other systems were examined to rule out any involvement. Serum biochemistries including complete blood count with platelet, bleeding time, clotting time, prothrombin time with INR, blood glucose, and renal and liver function tests were performed in all patients, while the titer of serum antibodies (ANA, ds-DNA) was evaluated in relevant cases.
We performed a biopsy from a representative lesion on the scalp for all patients. Punch biopsies (4 mm) were taken from the active margin of alopecic patches; vertical sectioning was done in most cases, while some required transverse sectioning (the biopsy sample was divided into two parts at the dermo-subcutaneous junction and embedded as two bits). All samples were stained with hematoxylin and eosin (H&E), while periodic-acid-Schiff was used when necessary, and studied under the microscope. Each sample was studied by an independent dermatopathologist (SS), who was blinded from the clinical diagnoses. Replacement of hair follicles by fibrous connective tissue was considered the histological hallmark of SA. Pus for culture and sensitivity was done in relevant cases, while potassium hydroxide examination was done to rule out tinea capitis (SSA). The biopsies were analyzed to assess the following changes—epidermal atrophy or hypertrophy, follicular plugging, basal cell degeneration, basement membrane thickening, the predominant type of derma inflammatory infiltrate (lymphocytes/neutrophils/mixed/absent or mild), dermal mucin deposition, and status of sebaceous glands. The final etiological diagnosis of PSA was made by clinico-pathological correlation.
Statistical analysis
Data was entered in a Microsoft Excel spreadsheet, and statistically analyzed using MedCalc® v17. We used mean and standard deviation (SD) (parametric data) and median [Inter-quartile range (IQR)] [non-parametric data] for descriptive statistics and proportion for categorical data. Normal distribution of numerical variables was determined using the Shapiro–Wilk test. Chi-square test was used for categorical data while the t-test and Mann–Whitney U test were applied for parametric and non-parametric data, respectively. A “P”-value <0.05 was considered significant.
| Results | | |
We diagnosed PSA in 61 patients during the study period among 66,370 patients attending our dermatology OPD, thus accounting for a prevalence of 0.09% (61/66,370). However, we included 53 patients in our study after fulfilling the inclusion and exclusion criteria and analyzing their data.
Fifty-three patients presented with PSA, diagnosed by clinico-pathological correlation. The most common subtype of PSA was LPP (39.6%, 21/53) [classical type: 20 cases, FFA variant 1 case] [Figure 1], followed by PBB (30.2%, 16/53) [Figure 2], discoid lupus erythematosus (16.9%, 9/53) [Figure 3], and non-specific SA (7.5%, 4/53), while CCCA, FD, and AKN accounted for 1 case each (1.9%) [Figure 4]. | Figure 1: (a) Clinical LPP (b) Perifollicular lymphocytic infiltrate, fibrosis (white arrow-head), and pigment incontinence (black arrow-head) (H and E, 100×)
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 | Figure 2: (a) Clinical PBB (b) Sparse superficial perivascular lymphocytic infiltrate with complete absence of hair follicles (H and E, 40×)
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 | Figure 3: (a) Scaly plaque of DLE (b) Sparse superficial and deep perivascular and periappendageal lymphocytic infiltrate; perifollicular fibroplasia [black arrow] (H and E, 40×)
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Demographic parameters
The mean age of our patients was 30.9 ± 8.1 years (range 1–50 years), more than half (52.8%, 28/53) belonging to 30–39 year age group. Overall, female predominance was noted (M: F 24:29), while male predilection was seen in PPB and non-specific SA. Only males developed FD and AKN, while CCCA and FFA affected females. The median duration before diagnosis was 4 years (range 2 months–36 years, IQR: 2–7 years, 95% CI: 3–5.2); maximum duration was noted as non-specific SA (18 years), while FFA showed the least duration (4 months) [P = 0.006, K-W test]. The majority of our patients had indoor jobs (52.8%, 28/53), except those with PPB, DLE, and AKN (P = 0.3, Chi-square). [Table 2] highlights the important demographic parameters.
Clinical features
Chronic insidious onset was most common in PPB (62.5%), DLE (88.9%), and all cases (100%) of CCCA, non-specific SA, SSA, and AKN, while LPP (85%), FD (100%), and FFA (100%) reported acute onset. (P = 0.001, Chi-square). Vertex was the commonest site of hair loss in all types of SAs with the following exceptions—frontal area in FD (100%), occipital area in AKN (100%), and equal affection of vertex, frontal, and temporal areas in DLE (33.3% each). The itching was the commonest symptom in subjects with LPP (55%), PPB (43.8%), FD (100%), and AKN (100%), while scalp pain was most common in DLE (66.7%). Interestingly, all patients (100%) with CCCA and non-specific SA remained asymptomatic. The solitary patient with FFA complained of both itching and pain. Perfollicular erythema was reported in all cases of DLE and FFA (P < 0.0001, Chi-square), while papule/pustule was significantly associated with FD and AKN (P = 0.0007, Chi-square). Scaling was seen in all patients with FFA (P = 0.05). Regarding clinical pattern, multiple-irregular patches were the commonest presentation in all disorders with SA (45.3%, 24/53) except DLE (single-large lesion-88.9%), CCCA (single-large lesion-100%), and all patients with FFA who presented with single-small lesions. The follicular presentation was the second most common clinical presentation overall, observed in DLE (55.6%, 5/9) and LPP (45%, 9/20). [Table 3] highlights the salient clinical features.
Nail involvement was noted in 20.7% (11/53) patients (onychomycosis[4] > longitudinal ridging[4] > dystrophy[3]), including all patients with non-specific SA (100%, 4/4), 35% (7/20) of those with LPP and a single patient (6.3%, n = 16) with PPB (P = 0.004, Chi-square). The patients with LPP revealed longitudinal ridging and nail dystrophy. Mucosal involvement was observed in 20.7% (11/55) subjects, mostly in those with LPP (5 cases), followed by DLE and PBB (3 cases each) (P = 0.8, Chi-square).
In the present study, 53 subjects reported 122 hair care practices, as almost 77.4% (41/53) consented to > 1 practice. Overall, non-medicated shampoo was used most frequently (94.3%, 50/53), followed by hair oil (92.4%, 49/55), hair color (33.9%, 18/53), and other physical modalities like straightening (hot comb) and hair braiding in five (9.4%) cases. No significant association was noted between the nature of hair care practice and the type of SA (primary or secondary) (P = 0.4, Chi-square).
Histopathological features
In the present study, the most frequent type of predominant inflammatory infiltrate was lymphocytic (88.7%, 47/53), followed by neutrophilic and mixed types in one (1.9%) case each, while absent/mild infiltrate was noted in 7.5% (4/53) cases. Overall, basal cell degeneration, interface dermatitis, and follicular plugging were the commonest histological changes in 50.9% (27/53) patients each. Basal cell degeneration was the commonest finding in LPP (90%, 18/20), DLE (88.9%, 8/9), and FFA (100%, 1/1) (P < 0.0001, Chi-square), while all patients (100%) with FFA, FD, and AKN demonstrated follicular plugging (P = 0.0001, Chi-square). Interface dermatitis was commonest in DLE (66.7%, 6/9), followed by PPB (56.3%, 9/16) and LPP (55%, 11/20). Regarding epidermal changes, epidermal atrophy was the commonest change in all disorders except epidermal hypertrophy in DLE (77.8%), FFA (100%), and AKN (100%). Basement membrane thickening and dermal mucin were noted only in DLE in 22.2% (P = 0.2, Chi-square) and 33.3% (P = 0.04, Chi-square) cases, respectively. Decreased/absent sebaceous glands were observed in all patients with FFA and FD, 12.5% patients with PPB, 22.2% DLE patients, and 20% patients with LPP (classical). (P = 0.2, Chi-square). The important histopathological characteristics are given in [Table 4].
We obtained clinico-pathological correlation for 69.8% (37/53) cases while the remaining 30.2% (16/53) showed discordance. Thirteen cases, clinically diagnosed as pseudopelade of Brocq, had revised final diagnosis after histology as LPP in nine cases and non-specific SA in the remaining four cases.
| Discussion | | |
In the present study (n = 53), the most common subtype of PSA was LPP (39.6%), followed by PPB (30.2%) and DLE (16.9%). There are very few Indian studies concerning primary cicatricial alopecia,[5],[6],[7] and none from the present setup, to our knowledge. All three Indian studies reported DLE to be the commonest cause of PSA in 41.7%, 79.2%, and 49% cases, respectively, while the prevalence of DLE was much low in our study (16.9%). Tan et al.[8] also noted DLE to be the commonest cause (33.9%), followed by PPB (24.1%) and LPP (22.3%). Our proportion of LPP (39.6%) is higher than Su et al.[1] and Trachsler and Trueb,[9] who reported LPP in 23.5% and in 26% cases, respectively. However, a study from Iran reported a much higher prevalence of LPP (69.7%).[10] We detected FFA in only one patient (1.9%), contrasting another Indian study (8.3%).[5] A study from Taiwan reported a higher prevalence of CCCA (12.4%), DC (30.3%), and AKN (12.4%), while we found a single case of CCCA and AKN each, while no case of DC was reported. Whiting[11] reported non-specific SA to be most frequent (40.6%), followed by LPP (12.6%) and FD (11.2%); however, we detected non-specific SA and FD in only 7.5% and 1.9% cases, respectively. These discrepancies may be attributed to the demographic and ethnic variation of different study populations and different clinico-pathological criteria for diagnosis of non-specific PSA.
We detected PPB in 30.2% cases, while different authors have reported a variable prevalence of this condition, ranging from 3.3% to 40.9%.[1],[5] This variation may have occurred as different definitions have been considered for this condition by various authors, as there are controversies regarding its pathogenesis. While some authors consider PPB and CCCA to be subtypes,[8],[12] others define PPB as the end stage of all PSAs after inflammation has burnt out.[13] However, the NAHRS classification considers both as distinct entities,[4] and we have followed this classification.
In the present study, the majority of patients were middle-aged belonging to 30–39 years age group, showing a female predilection (M: F 1:1.2) consistent with most previous studies[1],[8],[10],[11],[14], while some authors reported male preponderance.[5],[15],[16] Two Iranians reported a higher mean age of patients—39.1[10] and 37 years,[14] along with a Spanish study (53.5 years)[17]; in contrast, mean age of our patients was much lower—30.9 years (SD 8.1). Females are more likely to consult dermatologists for hair loss, due to their aesthetic concerns; thus explaining the female predominance in most studies. In the present study, age and gender had no significant association with the type of PSA, while Su et al.[1] have hinted a possible role of sex and age-related factors in the pathogenesis of these conditions. Our median disease duration before diagnosis was 4 years, almost double as that of a Spanish study (1.7 years),[17] but comparable to a study on African-American women (3.09 years)[18]; this may be attributed to ethnic variation and delayed presentation of our patients after trying all indigenous and local medications due to lack of awareness. Most of our patients had indoor jobs without any significant association with the diseases; this finding is in agreement with Beheshtiroy et al.[14] Notably, a study from Iraq demonstrated a significant association between PSA and outdoor occupation, possibly implying the role of sun exposure.[19]
Overall, vertex was the most commonest site of hair loss in our patients in 67.9% patients, while AKN involved only the occipital area and DLE showed more involvement in the frontal and temporal areas. Our findings are consistent with that of Su et al.[1] More than half of our patients (50.9%) reported chronic, insidious onset; in agreement with Villablanca et al.,[17] the itching was our commonest symptom in most disorders including LPP (55%), while pain was the commonest in DLE (66.7%) and CCCA, non-specific SA remained asymptomatic. However, Su et al.[1] reported itching to be the most commonest symptom in DLE and pain in dissecting cellulitis while most LPP patients remained asymptomatic. Perfollicular erythema (24.5%) and scaling (16.4%) were our commonest signs, in agreement with Su et al.[1] Multiple-irregular patches were our commonest clinical pattern/presentation (45.3%), followed by a follicular presentation (26.4%, LPP > DLE) and single-large patch (26.4%); in comparison a Spanish study reported follicular pattern to be the commonest, followed by single-large patch and multiple patches,[17] while multifocal-interconnected patches were deemed to be the commonest by a Taiwanese study.[1] Notably, single alopecic patch was the characteristic presentation of CCCA and DLE in our study, consistent with Su et al.[1] In the present study, 20.7% patients showed nail (non-specific SA > LPP) and mucosal involvement (LPP > DLE and PPB) each, which may serve as an additional clinical clue. We failed to find any comparator study in this regard. In our study, all patients reported at least one hair care practice, while 77.4% reported multiple hair care practices. Non-medicated shampoo was used most frequently (94.3%), followed by hair oil (92.4%), hair color (33.9%), and physical modalities like straightening (hot comb) and hair braiding in 9.1% cases. A study on African-American women also showed such high frequency of hair care practices, the most frequent being physical straighteners (hot comb) (96.3%), chemical straighteners (96.1%), and hair braiding (68.3%).[18] Hair color was used by 48.7% of their patients, comparable to our finding.[18] Traumatic hair care practices are more common in African-American women, because of their curly and difficult to comb hair, than in our patients who mostly used topical applications; although the former are becoming more popular. Traumatic hair care practices may lead to SA by inducing chronic, low-grade trauma.[18] Thus, we must counsel our patients to consult dermatologists for suitable hair care practices and avoid traumatic maneuvers.
Regarding histopathology, the majority of our patients (88.7%) demonstrated predominant lymphocytic inflammatory infiltrate, followed by neutrophilic and mixed types (1.8%) each, while 7.5% had mild/no infiltrate. Almost all previous studies have reported lymphocytic infiltration to be more common[1],[5],[8],[10],[11],[14],[17],[18] except a Chinese study which reported predominant neutrophilic infiltration.[16] In all patients, fibrous connective tissue replaced the hair follicles to variable degrees. Interface changes were most commonly observed in DLE (66.7%) > PPB (56.3%) > LPP (55%), in contrast, Thakur et al.[5] observed these changes in LPP (100%) > DLE (90%). Dermal mucin was noted only in DLE, consistent with previous studies.[5],[7] We observed absence/destruction of sebaceous glands in only 18.9% patients, in contrast, Inchara et al.[7] observed the same in 78.4% patients.
[Table 5] compares the salient features of some recent studies concerning PSA.
Limitations
Our study was limited by a small sample size, selection bias (as only histopathology confirmed PSA were included in a tertiary care setup), and cross-sectional study design, thereby preventing us from assessing the course and progression of these PSAs. Other important drawbacks were the lack of trichoscopy and failure to analyze the treatment modalities or therapeutic advantages. We also failed to conclude how to distinguish these disorders by histopathology and thus suggest clinic-pathological correlation in such cases.
| Conclusion | | |
To conclude, PSAs are a heterogeneous group of disorders with varying degrees of clinical overlap and pose a diagnostic dilemma for dermatologists. So, for accurate diagnosis histopathology should be performed in every case, and clinically correlated. This disorder predominantly affected middle-aged women. In our patients, LPP was the commonest etiology/subtype, followed by PPB and DLE while lymphocytic infiltration was most predominant histologically. The delayed presentation might be a possible reason for predominant lymphocytic infiltrate in most of our patients. Thus, patients should be encouraged to present to the dermatologist early in the course of disease to enable accurate diagnosis and appropriate treatment. Nail and mucosal involvement are additional diagnostic clues for LPP, while perifollicular erythema may be considered a clinical marker for DLE. Histologically, basal cell degeneration was significantly associated with DLE, LPP, and FFA while dermal mucin deposition was specific for DLE. Although hair care practices may have a contributory role, there is no statistically significant association. The authors recommend further large-scale studies involving the genetics and patho-mechanisms of these disorders, which may help to classify the subtypes of PSAs more elaborately. A dearth of a similar literature in the present study has prompted this study.
Acknowledgement
The authors would like to acknowledge the help of Dr. Swosti Mohanty, Assistant Professor, Era Medical College and Hospital, Lucknow, Uttar Pradesh in obtaining some of the histopathologic images.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
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| 2. | Chiang YZ, Bundy C, Griffiths CE, Paus R, Harries MJ. The role of beliefs: Lessons from a pilot study on illness perception, psychological distress and quality of life in patients with primary cicatricial alopecia. Br J Dermatol 2015;172:130-7. |
| 3. | Conic RR, Piliang M, Bergfeld W, Atanaskova-Mesinkovska N. Vitamin D status in scarring and non-scarring alopecia. J Am Acad Dermatol 2018;85:478-80. |
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| 5. | Thakur BK, Verma S, Raphael V. Clinical, trichoscopic, and histopathological features of primary cicatricial alopecias: A retrospective observational study at a tertiary care centre of North East India. Int J Trichology 2015;7:107. |
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| 9. | Trachsler S, Trüeb RM. Value of direct immunofluorescence for differential diagnosis of cicatricial alopecia. Dermatology 2005;211:98-102. |
| 10. | Fatemi-Naeini F, Mokhtari F, Saber M, Basiri A, Matin M. An epidemiological study of 198 cases of primary cicatricial alopecia in Iran. J Adv Med Res 2017;11:1-6. |
| 11. | Whiting DA. Cicatricial alopecia: Clinico-pathological findings and treatment. Clin Dermatol 2001;19:211-25. |
| 12. | Sperling LC, Solomon AR, Whiting DA. A new look at scarring alopecia. Arch Dermatol 2000;136:235-42. |
| 13. | Amato L, Mei S, Massi D, Gallerani I, Fabbri P. Cicatricial alopecia; A dermatopathologic and immunopathologic study of 33 patients (pseudopelade of Brocq is not a specific clinico-pathologic entity). Int J Dermatol 2002;41:8-15. |
| 14. | Beheshtiroy A, Hajmanoochehri F, Hossienghamar F. An epidemiological study of 97 cases of primary cicatricial alopecia in Iran. Dermatol Rep 2015;7:59-60. |
| 15. | Nejad SB, Khodaeiani E, Amirinia M, Goldust M. Evaluation of cicatricial alopecia in Iran. Pak J Biol Sci 2013;16:1609-11. |
| 16. | 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 2014;80:306-12. [ PUBMED] [Full text] |
| 17. | Villablanca S, Fischer C, García-García SC, Mascaró-Galy JM, Ferrando J. Primary scarring alopecia: Clinical-pathological review of 72 cases and review of the literature. Skin Appendage Disord 2017;3:132-43. |
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[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5] |
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