Evaluation of Clinical Significance of Dermoscopy in Alopecia Areata

DERMOSCOPY ROUND

Evaluation of Clinical Significance of Dermoscopy in Alopecia Areata Akhila Sai Guttikonda, Chintaginjala Aruna, D V S B Ramamurthy, K Sridevi, Senthil Kumar L Alagappan

Abstract From the Department of Background: Alopecia areata (AA) is a common, chronic inflammatory disease characterized Dermatology, Venereology, by nonscarring hair loss on the scalp or any hair‑bearing area of the body. Recently, Leprology, Katuri Medical dermoscopy, a noninvasive diagnostic procedure, has been employed for the diagnosis of AA. College and Hospital, Guntur, Andhra Pradesh, India Aim: To evaluate various dermoscopic patterns in AA and correlate these patterns with the disease activity and severity. Materials and Methods: Dermoscopy was performed on AA patients using DL1 dermoscope (magnification ×10 was used). The dermoscopic patterns Address for correspondence: recorded were analyzed to identify any correlation with the disease activity and severity. Dr. Chintaginjala Aruna, Results: A total of fifty patients of AA were recruited in the study. Female outnumbered Department of Dermatology, males with the ratio being 1.173:1. Mean age of the patients was 25.06 years. Mean duration Venereology, Leprology, of disease was 14 months. The most common site involved was scalp (80%) and type noted Katuri Medical College and Hospital, Guntur ‑ 522 019, was patchy (84%). Various dermoscopic patterns noted were yellow dots (YD) (88%), short Andhra Pradesh, India. vellus hair (66%), black dots (BD) (58%), broken hairs (BHs) (56%), tapering hair (TH) (26%), E‑mail: [email protected] Coudability hairs (14%), pigtail hair (14%), and Pohl‑Pinkus constrictions (2%). Statistically significant correlation was observed between BD, BHs, THs, and disease activity. No significant correlation was found between severity and any of the dermoscopic features. Conclusion: The most common dermoscopic pattern in our study was YD. Presence of BDs, BHs, and THs indicate active disease. Dermoscopic patterns were not affected by severity of the disease.

Key Words: Alopecia areata, black dots, dermoscopy, micro exclamation mark hair, yellow dots

What was known? Various dermoscopic features in alopecia areata are black dots (cadaverous hairs), yellow dots, tapering hairs (exclamation mark hairs), and broken hairs.

Introduction smooth surface and characteristic exclamation mark hair. Alopecia areata (AA) is a common, chronic inflammatory In the past, doubtful cases were confirmed by invasive disease characterized by nonscarring hair loss on procedures such as punch biopsy, which at times can the scalp or any hair‑bearing area of the body. It be troublesome in pediatric age group. This problem accounts for 25% of all alopecia cases presenting to has been overcome by dermoscopy, a noninvasive the dermatologists and 2–3% of all new outpatient diagnostic procedure, which magnifies subtle clinical dermatology services in the USA and the UK, 3.8% in surface features of skin lesions as well as unveils some China, and 0.7% in India.[1‑4] Although AA may occur at subsurface skin structures normally not visible even [6] any age, incidence is high among younger age group; in with a magnifying lens. Various dermoscopic features fact, it is the most common form of alopecia seen in in AA that are already described in the literature are children. Various patterns of alopecia described clinically black dots (BD) (cadaverous hairs), yellow dots (YD), are patchy, diffuse, reticulate, ophiasis, ophiasis inversus, tapering hairs (THs) (exclamation mark hairs), broken [7] and depending on the extent of hair loss, alopecia hairs (BHs), etc. With this background, we conducted subtotalis, alopecia totalis (complete loss of scalp hair), a study to evaluate various dermoscopic patterns in AA and alopecia universalis (complete loss of body hair) are that help in diagnosis and to correlate these patterns described.[5] with disease activity and severity so that ideal treatment can be planned. AA is diagnosed clinically by the presence of well‑circumscribed, round, or oval bald patches with This is an open access article distributed under the terms of the Creative Commons Attribution‑NonCommercial‑ShareAlike 3.0 License, which allows Access this article online others to remix, tweak, and build upon the work non‑commercially, as long as the Quick Response Code: author is credited and the new creations are licensed under the identical terms. Website: www.e‑ijd.org For reprints contact: [email protected]

How to cite this article: Guttikonda AS, Aruna C, Ramamurthy D, Sridevi K, Alagappan SL. Evaluation of clinical significance of dermoscopy DOI: 10.4103/0019-5154.193668 in alopecia areata. Indian J Dermatol 2016;61:628-33. Received: May, 2015. Accepted: August, 2016.

Materials and Methods and severity of scalp hair loss. The dermoscopic patterns We conducted a cross‑sectional study on all AA patients recorded were analyzed to identify a correlation between attending to the outpatient department of our hospital any of the specific dermoscopic features and the disease from January 2013 to September 2014 after obtaining activity and severity by Spearman rank‑order correlation Institutional Ethical Committee clearance. All the patients coefficient by rank test and their statistically significant with AA irrespective of age and sex who were willing was determined by calculating P value. to undergo the protocol were included in the study. An Results informed consent was obtained from the patient or parent or guardian in case of a child. Cases of AA were clinically Fifty patients of AA were recruited in the study. Most of diagnosed, and biopsy was done in ambiguous cases. the patients (86%) were younger than 40 years. There Epidemiological data (name, age, sex, and occupation), was an extreme variation in the duration of the disease, relevant history (age of onset, duration of the disease, ranging from 10 days to 8 years. The alopecia remained history of atopy, association with other autoimmune confined to the scalp in 72% (36/50) of the cases, only diseases, and family history), and clinical examination body hair was involved in 20% (10/50), and both were including general, systemic, and cutaneous examinations involved in 8% (4/50) of the cases. Most common type were documented. Biopsy was done in two cases to confirm of AA in our study was patch type. Localized patches the diagnosis. A number of patches, distribution, pattern, (1–3) were seen in 70% (35/50) of the cases and morphology, and characteristic features if any were noted. multiple patches (>3 patches) were seen in 14% (7/50) of the cases. Demographic and clinical details were given Dermoscopic patterns of the patches were noted with the in Table 1. In the present study of fifty patients, there help of DL1 dermoscope (DermLite, 3 Gen LLC, San Juan Capistrano, CA, USA) (magnification × 10) that can be used without immersion oil because of the presence of Table 1: Demographic and clinical characters of study polarized filters. Dermoscope was attached to Samsung population Galaxy S3 smartphone with an adaptor [Figures 1 and 2]. Character Values Dermoscopic features were observed, and the photographs Sex (female to male ratio) 1.173:1 were taken with the help of camera of mobile device. Age (mean±SD), years 25.06±12.08 Later, they were transferred to the laptop and were Disease duration (mean±SD), months 14±20 stored for further comparison and analysis. Assessment Positive family history of the disease, % 10 (5/50) of disease activity was based on the subjective history Association with atopy, % 32 (16/50) of progression and an objective evaluation of hair pull History of associated thyroid 8 (4/50) test at the margins of each individual patch. Severity of abnormalities, % disease was assessed by severity of alopecia tool (SALT) Various patterns of alopecia, % score calculated based on the combination of extent Patchy 84 (42/50) Reticulate 6 (3/50) Ophiasis 6 (3/50) Diffuse 4 (2/50) Site of involvement, % Scalp 80 (40/50) a Beard area 18 (9/50) Eye brow 2 (1/50) SD: Standard deviation b

c Figure 1: (a) Cross‑polarized spacer unit (b) DL1‑dermacope (c) Samsung Galaxy S3 mobile phone, attached to DermLite mobile device case Figure 2: DermLite DL1 ‑ dermoscope attached to mobile phone

629 Indian Journal of Dermatology 2016; 61(6) Guttikonda, et al.: Dermoscopy in alopecia areata were a total of 109 patches and hair pull test was done in 2004. Since then, it was widely used in this field at the margins of each individual patch to assess the because of its ease and noninvasiveness. activity. It was positive in 35% (38) of the patches and Table 2 depicts the comparison of dermoscopic features negative in 65% (71) of the patches. Grade S1 severity of our study with other Indian studies and with the was found in 58% of the study population as determined study done in Japan. by SALT score, the details were represented in Figure 3. Dermoscopic evaluation of the scalp in the current Yellow dots study revealed different hair shaft abnormalities and They represent distended follicular orifices of the various patterns at hair follicle openings against the affected follicles, filled with sebum and keratinous background of honeycomb pigment network. The most material. They appear as round or polycyclic, yellow to common finding was YDs followed by short vellus yellow‑pink dots devoid of hairs or contain miniaturized hair (SVH) [Table 2 and Figures 4‑9]. Micro‑exclamation or cadaverized or dystrophic hairs. In our study, YDs mark hair was seen in 16% (8/50) of the cases. were seen in 88% (44/50) of cases, similar to the Statistically significant correlation was observed between other studies.[9‑11] However, some studies reported BD, BHs, TH, and disease activity. SVHs correlated lesser incidence.[7,12,13] This variation in results can be negatively with the disease activity, but this was attributed to the difference in skin types (yellowish not statistically significant [Table 3]. No significant color of skin in Asians may make it difficult to perceive correlation was found between the severity and any of the YDs on dermoscopy), different shampooing habits, the dermoscopic features [Table 4]. and difference in the type of dermoscope used.[7,14] In view of their higher frequency in AA as reported by Discussion various studies including ours, YD can be regarded as a Dermoscopy has been established as an essential tool sensitive marker for the diagnosis of AA. in the diagnosis of various hair disorders. Lacarrubba et al.[8] first described videodermoscopic features of AA

Figure 3: Severity of alopecia areata determined by severity of alopecia tool score

Figure 4: Yellow dots (×10)

Figure 5: Black dots (red arrow), broken hairs (blue arrow), and tapering hairs (green arrows) (×10) Figure 6: Short vellus hairs (×10)

Indian Journal of Dermatology 2016; 61(6) 630 Guttikonda, et al.: Dermoscopy in alopecia areata

Table 2: Comparison of dermoscopic features of alopecia areata with other studies Features at hair Present Inui et al.[7] Mane et al.[10] Peter et al.[13] Hegde et al.[12] follicle openings study(%) (Japan),% (India), % (India), % (India), % YD 44 (88) 63.70 81.80 42 57.30 BD 29 (58) 44.30 67.70 75 84 Hair shaft abnormalities SVH 33 (66) 72.70 40.90 57.14 68 BH 28 (56) 45.70 55.40 67 37.33 TH 13 (26) 31.70 12.10 33.33 18.67 CH 7 (14) NM NM NM NM PTH 7 (14) NM NM 17.50 NM PPC 1 (2) NM 3 NM NM NM: Not mentioned, YD: Yellow dots, BD: Black dots, BH: Broken hair, TH: Tapering hair, SVH: Short vellus hair, CH: Coudability hairs, PTH: Pigtail hair, PPC: Pohl‑Pinkus constriction

Table 3: Correlation of activity of alopecia areata with dermoscopic findings Disease activity (number of patches) YD (%) BD (%) BH (%) TH (%) SVH (%) CH (%) PTH (%) PPC (%) Present (38) 31 (81.5) 34 (89.4) 28 (73.6) 22 (57.8) 14 (36.8) 6 (15.7) 2 (5.2) 1 (2.6) Absent (71) 58 (81.6) 14 (19.7) 14 (19.7) 4 (5.6) 38 (53.5) 4 (5.6) 4 (5.6) 0 Total (109) 89 (81.6) 48 (44) 42 (38.5) 26 (23.8) 52 (47.7) 10 (9.1) 6 (5.5) 1 (0.9) Correlation co‑efficient −0.001 0.67 0.528 0.584 −0.159 0.168 −0.008 0.132 P 0.989 (NS) 0 (S) 0 (S) 0 (S) 0.098 (NS) 0.081 (NS) 0.0936 (NS) 0.173 (NS) YD: Yellow dots, BD: Black dots, BH: Broken hair, TH: Tapering hair, SVH: Short vellus hair, CH: Coudability hairs, PTH: Pigtail hair, PPC: Pohl‑Pinkus constriction, S: Significant, NS: Not significant

Table 4: Correlation of severity of alopecia areata with dermoscopic features Severity (number of patients) YD (%) BD (%) BH (%) TH (%) SVH (%) CH (%) PTH (%) PPC (%) S1 (29) 27 (93) 16 (55) 15 (51) 8 (27.5) 21 (72) 4 (13.7) 6 (20.6) 1 (3.4) S2B0 (2) 1 (50) 2 (100) 1 (50) 0 2 (100) 0 1 (50) 0 S2B1 (1) 0 0 1 (100) 0 1 (100) 0 0 0 S3B0 (5) 4 (80) 5 (100) 5 (100) 4 (80) 4 (80) 2 (40) 0 0 S3B1 (1) 0 1 (100) 1 (1) 1 (100) 0 1 (100) 0 0 S4B0 (1) 0 1 (100) 1 (100) 1 (100) 0 0 0 0 S4B1 (1) 0 0 1 (100) 0 0 0 0 0 B1 (10) 10 (100) 4 (44.4) 3 (30) 3 (30) 6 (60) 0 0 0 Total (50) 42 (84) 29 (58) 28 (56) 17 (34) 34 (68) 7 (14) 7 (14) 1 (2) Correlation co‑efficient 0.125 0.024 0 0.078 0.148 0.017 0.257 0.116 P 0.387 (NS) 0.871 (NS) 1 (NS) 0.59 (NS) 0.305 (NS) 0.907 (NS) 0.072 (NS) 0.421 (NS) YD: Yellow dots, BD: Black dots, BH: Broken hair, TH: Tapering hair, SVH: Short vellus hair, CH: Coudability hairs, PTH: Pigtail hair, PPC: Pohl‑Pinkus constriction, NS: Not significant

Black dots (cadaverous hairs) as trichotillomania. In AA, usually hairs are broken They are the remnants of BH and TH. BD is difficult to at the same level above the skin surface, whereas in appreciate in Caucasians due to the hair color. In our trichotillomania, every BH has a different length.[15] study, BD was seen in 58% of the cases, and the result In our study, BH was seen in 56% of the cases on par was comparable to that of Karadag Köse and Güleç[11] with Mane et al.[10] study. Some studies reported lesser and Mane et al.[10] incidence.[7,11,12] These variations in results may be due to difference in activity, severity, and duration of the Broken hairs disease in various studies.[15] BH results either from the transverse fracture of terminal hair shafts weakened by the inflammatory process or by Tapering hairs (exclamation mark hairs) rapid regrowth of incompletely destroyed hair shafts They represent fractured hairs with frayed thicker distal that previously formed the BDs. They are not specific end and thinner proximal shaft. Clinically visible TH is to AA as they are also seen in other conditions such of approximately 1 cm long, whereas dermoscopy aids

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in only 5 (10%) cases but with dermoscopy they (micro‑exclamation mark hairs) were found in additional 8 (16%) cases (total of 13 patients [26%]). Thus, dermoscopy was more sensitive in picking up TH than the naked eye and as this finding indicates active disease,[7] ideal treatment plan can be tailored. Studies of Inui et al.[7] and Peter et al.[13] reported slightly higher incidences of TH. Coudability hairs They were initially described by Shuster in 1984, as normal looking hairs that can be made to kink easily when bent or pushed inward.[16] An interesting hypothesis was that coudability hairs (CH) precede BD and TH, as it appears in seemingly intact hairs of normal length. Figure 7: Coudability hairs (×10) They were seen in 14% of cases in the present study, compared to 12–42% reported by Rudnicka et al.[15] Short vellus hairs and pigtail hairs Lacarrubba et al.[8] described two patterns of hair regrowth in some patients with chronic AA, one was homogeneous and <10 mm long hair indicating early disease remission (upright vellus hair) and second was sparse, thin and twisted vellus hair with characteristic circular hair pattern pigtail hair (PTH) that were usually lost after few weeks. Regrowth of SVH after treatment can be seen in dermoscopy even before they can be perceived by the naked eye. In the present study, SVH was seen in 66% of the patients, similar to Hegde et al.[12] study. Peter et al.,[13] and Mane et al.[10] found a lower incidence of SVH. This variation in the incidences may be attributed to the difference in exposure of patients to various treatment modalities before being included Figure 8: Pigtail hairs (×10) in the study. PTH was seen in 14% of the patients in the current study, whereas Peter et al.[13] reported it in 17.5% of the patients. As there were very few studies reporting PTH incidence, further studies with large sample size and follow‑up are necessary to comment on its evolution and prognostic significance. Pohl‑Pinkus constrictions They represent constrictions in the hair shafts at irregular intervals. Repeated formation of these Pohl‑Pinkus constrictions (PPC) during the course of disease activity results in the formation of monilethrix‑like hairs. In our study, PPC was observed in one patient and Mane et al.[10] reported in two of his patients. Correlation between dermoscopic features and disease activity In the present study, disease activity assessed by hair Figure 9: Pohl‑Pinkus constriction (×10) pull test of each patch correlated positively with BD, BH, and TH. SVH correlated negatively with the disease in visualizing exclamation mark hairs of even 1–2 mm activity, but this was not statistically significant. Positive long, the latter are referred to as “micro‑exclamation correlation was observed earlier[7] and the present study mark hairs.” On clinical examination, TH was seen further confirms that. Peteret al.[13] did not find any

Indian Journal of Dermatology 2016; 61(6) 632 Guttikonda, et al.: Dermoscopy in alopecia areata correlation with the disease activity. Positive correlation Financial support and sponsorship in the present study with BD, BH, and TH can be Nil. explained on the basis that they represent distinct but similar ways, in which the hair follicle responds to Conflicts of interest an initial inflammatory insult at the hair bulb region. There are no conflicts of interest. Initially, a constriction (PPC) occurs in the mid part of the proximal hair shaft, later proximal end of these hairs What is new? Micro‑exclamation mark hairs are a marker of disease activity can be demonstrable becomes thinner than the distal end (CH). Sometimes, only with the help of dermoscopy. Presence of black dots, broken hair, and tapering CH may regain normal thickness with cessation of an hair indicate active disease. inflammatory insult, or these hairs may eventually break resulting in BH or TH, and if the inflammatory insult is References continuous, hair shafts become progressively thinner and 1. McMichael AJ, Pearce DJ, Wasserman D, Camacho FT, break at the level of scalp to form a BD. Thus, BD, BH, Fleischer AB Jr., Feldman SR, et al. Alopecia in the United States: Outpatient utilization and common prescribing and TH are the result of most severely affected follicles, patterns. J Am Acad Dermatol 2007;57 2 Suppl: S49‑51. whereas CH and PPC are the result of least severely 2. Safavi KH, Muller SA, Suman VJ, Moshell AN, Melton LJ 3rd. affected follicles. Absence of correlation between CH Incidence of alopecia areata in Olmsted County, Minnesota, and PPC and the disease activity in the present study 1975 through 1989. 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Tosti A, Duque‑Estrada B. Dermoscopy in hair disorders. signs of disease activity were seen in some clinically J Egypt Womens Dermatol Soc 2010;7:1‑4. inactive patches in our study, thus helping us to pick up 15. Rudnicka L, Olszewska M, Rakowska A, Slowinska M. Atlas of Trichoscopy: Dermoscopy in Hair and Scalp Disease. London: more active patches which were not identified clinically Springer‑Verlag; 2012. or by positive hair pull test, thus enabling active 16. Shuster S. ‘Coudability’: A new physical sign of alopecia intervention at an earlier date. areata. Br J Dermatol 1984;111:629.

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