Hair and scalp disorders in women of African descent: an overview A. Salam, 1 S. Aryiku 2 and O.E. Dadzie 3

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1 REVIEW ARTICLE BJD British Journal of Dermatology Hair and scalp disorders in women of African descent: an overview A. Salam, 1 S. Aryiku 2 and O.E. Dadzie 3 1 Imperial College Healthcare NHS Trust, London, U.K. 2 Nottingham University Hospitals NHS Trust, Nottingham, U.K. 3 Department of Dermatology and Histopathology, The North West London Hospitals NHS Trust, Northwick Park Hospital, Watford Road, Harrow, HA1 3UJ, U.K. Summary Correspondence Ophelia E. Dadzie. opheliadadzie@nhs.net Accepted for publication 18 June 2013 We present an overview of hair and scalp disorders in women of African descent, discussing the biological features of afro-textured hair, as well as hair-grooming practices in this cohort and their association with specific hair and scalp disorders. A practical approach to diagnosing and managing common hair and scalp disorders in this cohort is also presented. Funding sources This supplement was kindly sponsored by L Oreal Research & Innovation and Beiersdorf. Conflicts of interest O.E. Dadzie has received funding from L Oreal to support a study on alopecia in women of African descent. The other authors have not declared any conflicts of interest. DOI /bjd What s already known about this topic? Hair and scalp disorders are a significant problem in women of African descent. What does this study add? An overview of the biological characteristics of afro-textured hair. An overview of the hair-grooming practices of women of African descent. A practical approach to diagnosing and managing common hair and scalp disorders in women of African descent. Global population forecasts from the U.S. Central Intelligence Agency indicate that of the 15 billion people that the world is predicted to have gained by 2020, 16% will be from Africa. 1 Similar (albeit smaller) changes have also been observed in several Western countries. For example, the U.K. has seen the proportion of Black-Africans double between 2001 and Alongside the current and predicted changes in the global population, the ethnic hair industry is worth billions of dollars. 3,4 Several epidemiological and hospital-based studies have shown that hair and scalp disorders are a significant problem in people of African descent. In light of this, as well as the current and predicted changes in global demographics, there is an increasing need for clinicians to be cognizant of hair and scalp disorders in people of African descent. Methods We identified relevant articles through a systematic online literature search (PubMed, ). The search utilized Boolean operators and was designed to be both broad and inclusive. Key search terms included: (hair OR follicle OR scalp OR shaft OR alopecia OR cicatricial OR scarring OR vertex OR haircare) AND (African OR Africa OR Afro OR black OR ethnic OR dark OR pigment OR pigmented). Relevant titles, abstracts and full articles identified from the search were reviewed and included if pertinent to hair and scalp disorders in women of African descent. Additional articles were also retrieved from the cited reference list of articles identified from our initial systematic online literature search. Throughout this review the term afro-textured hair is used to imply the spectrum of naturally curly hair occurring in African-Americans, Afro-Carribeans and indigenous African women. 4 Classification of human hair Human hair has traditionally been classified into three major groups (African, Asian and Caucasian) based on macroscopic characteristics. However, this does not take into account the variability seen within and between genetically distinct groups. 19

2 20 Hair and scalp disorders in women of African descent, A. Salam et al. Loussouarn et al. 5 have developed a new method of classifying human hair based on objective assessment of hair shape. Using this system, they have classified human hair into eight groups, independent of race and/or ethnicity (Fig. 1). Their classification system shows clearly the diverse hair phenotypes of women of African descent. Understanding how and why this diversity evolved is important, but is an area that has been relatively unexplored by scientists. Biology of afro-textured hair The physical and chemical properties of all human hair types are very similar. 6 However, there are distinct biological and structural differences in relation to afro-textured hair. 7 These include: (i) an elliptical or kidney bean -shaped hair shaft, situated eccentrically within the follicular epithelium (Fig. 2) 8 ; this contrasts with the circular or slightly oval-shaped hair shaft of Caucasian hair; (ii) retrocurvature of the hair follicle (with a golf club-shaped bulb), in contrast to the straight shape of Caucasian follicles 9 the bulb appears to be crucial in determining hair curliness; this has been shown to be linked to an asymmetry in differentiation programmes in this structure 9,10 ; (iii) lower moisture content has been suggested, although the evidence for this is limited; 11 (iv) formation of both complex (involves two or more hair fibres) and singlestrand knots; 12 these intertwined hair fibres are difficult to comb and hence susceptible to breakage during normal grooming of the hair; (v) a slower hair growth rate compared with Caucasian and Asian hair (mean SD, , and lm daily, respectively), with more hairs being found in the telogen phase, especially in the occipital and temporal regions; 13,14 (vi) reduced total hair density and number of terminal anagen follicles 15 this is relevant when setting the quantitative threshold for diagnosing alopecia on scalp biopsies. It is important to note that these aforementioned characteristics represent broad generalizations that do not take into account the within-group variability of this hair phenotype. Hair grooming The hair styles of women of African descent can be divided broadly into two groups: natural vs. chemically treated hair. 16,17 Natural hairstyles include the afro, dreadlocks, twisting and braiding (Fig. 3a). The latter can be undertaken with or without the use of human or artificial hair extensions. Hot combs can also be used to straighten afro-textured hair temporarily. Chemical processing (Fig. 3b) of afro-textured hair is Fig 1. A new method for classifying human hair based on objective assessment of hair shape. This novel classification system demonstrates the within and between group variability of human hair. Reproduced from Loussouarn et al., 5 with permission from Wiley-Blackwell.

3 Hair and scalp disorders in women of African descent, A. Salam et al. 21 (a) Fig 2. Horizontal section of a scalp biopsy showing the elliptical or kidney bean -shaped hair shaft of afro-textured hair. Note: the hair shaft is eccentrically located in the follicular epithelium (haematoxylin and eosin stain; original magnification: 9100). (b) a common practice, with one study reporting that 50% of black South African women relax their hair. 18 Traditional salon relaxers ( lye relaxers ) are emulsions of 15 35% sodium hydroxide (ph range 12 14). 19 Base-lye relaxers are higher ph lye relaxers that require a protective base coat of petrolatum to be applied to the scalp. No-lye relaxers (potassium hydroxide, lithium hydroxide or guanidine hydroxide), and thio relaxers (ammonium thioglycolate) are also available for home use. During the process of chemical relaxation of afro-textured hair, these aforementioned hydroxide emulsions are applied to the hair. This leads to breakage of disulfide bonds and softening and stretching of the hair shaft. 20 The straight shape of the hair is fixed by rinsing with an oxidizing agent. A neutralizing shampoo is then used to bring the hair back to its physiological ph. This step is imperative, as ongoing contact with the chemical relaxer will cause complete disintegration of the hair strands. Finally, a conditioning shampoo is used to restore moisture to the hair. Chemical straightening of afro-textured hair is not permanent; new growth will possess the original disulfide bonds and for this reason regular touch ups are advised (preferably not more frequently than eight weekly). Weaves, wigs and hair extensions are also used by women of African descent as fashionable pieces, and protective styling methods, in association with their natural or chemically processed hair (Fig. 3c). Given the costs involved in visiting professional stylists, some women may choose to style and/or groom their own hair. (c) Fig 3. (a) Afro-textured hair is braided as single plaits using artificial hair extensions. (b) Chemically relaxed afro-textured hair; the normal curl is lost, with the hair now appearing straight and soft. (c) Sewn-in weave; human or artificial hair extensions are sewn onto corn-rowed natural hair. Courtesy of Dr Camille Fitoussi. Reprinted from Dadzie et al., 4 with permission from Wiley-Blackwell.

4 22 Hair and scalp disorders in women of African descent, A. Salam et al. Others may rely on friends and/or relatives. Using untrained individuals to groom hair may lead to further hair damage. Hair-grooming practices and the link with hair and scalp disorders The evidence linking hair-grooming practices with specific hair and scalp disorders in women of African descent is rather variable and difficult to prove. This is because many in this cohort would have worn different hairstyles throughout their lifetime. To date the evidence indicates: (i) a link between traction alopecia (TA) and hairstyles that induce prolonged tension on the hair root, e.g. dreadlocks, weaves and braiding; the risk is highest in the setting of combined hairstyles, i.e. braiding chemically relaxed hair; 21 (ii) a link between the use of sewn-in hair weaves and cornrow or braided hairstyles with artificial hair extensions and central centrifugal cicatricial alopecia (CCCA) 22 ; (iii) a link between hair fragility and the use of chemical relaxers this was demonstrated by the work of Khumalo et al., 23 who undertook biochemical analysis of natural asymptomatic and symptomatic (brittle) relaxed hair. They found that there was a decrease in cystine, citrulline and arginine in all relaxed hair compared with natural hair; the cysteine levels in distal asymptomatic relaxed hair and all symptomatic (brittle) relaxed afro-textured hair were similar to each other, and to those observed in the genetic hair fragility disorder, trichothiodystrophy; 23 (iv) the development of irritant contact dermatitis and rarely Stevens Johnson syndrome with the use of chemical relaxers; 24,25 (v) anaphylactic and allergic contact reactions can occur to glues and other adhesives used to attach weaves/hair extensions to the natural hair. 26,27 Epidemiology of hair and scalp disorders in women of African descent Most of the prevalence data pertaining to hair and scalp disorders in people of African descent have been obtained from studies undertaken within hospital settings. However, such data are often biased, not representative of the general population and often based on small sample sizes. For this reason, community-based studies are preferable. To date, both hospital and community studies undertaken in the U.K., 28 U.S.A., France, 32 Senegal, 33 Nigeria, 34,35 Burkina Faso 36 and South Africa 18,37 have shown that hair and scalp diseases, are a significant problem in people of African descent. These studies also indicate that both scarring and nonscarring alopecia occur in women of African descent. Further data pertaining to the frequency of specific hair and scalp disorders occurring in women of African descent are available from four community studies: two from South Africa 18,37 and two from the U.S.A. 30,31 The two South African studies 18,37 investigated hair and scalp disorders in 1042 African school children (aged 6 21 years) 37 and 874 adults (aged years). 18 The prevalence of TA was found to be 17% in schoolgirls, but higher (32%) in adult women. Folliculitis keloidalis nuchae (FKN) was diagnosed in 47% of final-year schoolboys, 11% of adult men, but only in 02% of adult women. In contrast CCCA was not found in schoolgirls, but was diagnosed in 27% of adult women. This figure increased to 54% in women aged > 50 years. Tinea capitis was identified in 19% of first-year school children, 72% of which was in boys, but among older schoolchildren only 06% were diagnosed with the condition. In both of the South African studies, histopathological assessment was not undertaken, thus subjects were diagnosed based on clinical assessment only. The two North American studies 30,31 evaluated the prevalence of hair loss in African-American women. The first 30 involved 529 participants from six study sites including a hair and beauty symposium, two church groups and three standalone workshops. The symposium and church groups had a 56% point prevalence of CCCA, but at the three stand-alone workshops this was 16%, demonstrating how sampling techniques can impact results. The second study, 31 including 326 subjects from two churches and a health fair, reported a prevalence of CCCA of 17%. The two North American studies used a validated photographic scale to diagnose CCCA, but again the findings were not supported by histopathological assessment. Further epidemiological studies in different geographical regions, using both clinical and histopathological findings, are required to appreciate better the true prevalence of different hair and scalp disorders in women of African descent. Clinical assessment A few principles should guide the assessment of women of African descent presenting with disorders of the hair and scalp. Firstly, there may be more than one concomitant diagnosis (e.g. CCCA and seborrhoeic dermatitis or CCCA and TA) (Fig. 4a,b). Secondly, scarring may not always be appreciated clinically. For this reason, there should be a low threshold for performing scalp biopsies, which should be reported, preferably by a pathologist/dermatopathologist, trained in the histopathological interpretation of scalp biopsies. History Aside from the standard history obtained in all cases of alopecia, specific questions are required regarding hair-grooming practices in this cohort. Examples of pertinent questions are shown in Table 1. A more comprehensive 36-point questionnaire has been developed by one of the authors (O.E.D.): the London Hair Grooming Assessment Instrument. This latter tool is of particular use in the research setting. Taking a detailed hair-grooming history is important as it guides how patients are counselled regarding minimizing their adverse hair care practices. 16 Examination Examination of the scalp should be undertaken in good lighting, and should also include complete physical examination of the rest of the integument, including skin, nails and mucosae.

5 Hair and scalp disorders in women of African descent, A. Salam et al. 23 (a) (b) Table 1 Hair care history (pertinent questions) What is your current hairstyle? How many different hairstyles have you had since childhood? What hairstyle have you worn the longest? How often do you change your hairstyle? Do you visit a professional stylist for your hair grooming and styling? Do you, your friends, or your family style your hair? Which at-home maintenance products do you use? How often do you normally wash your hair? Do you use a blow dryer or sit under a hair dryer? Is your hair chemically treated/do you have a relaxer? If so, how often do you reapply the relaxer to the new growth (touch up)? At what age did you first start using chemical relaxers? Do you colour your hair? If so, do you colour your hair and use a chemical relaxer concurrently? Do you wear weaves? If so, is your weave sewn or glued in? Do you braid your hair? If so, do you braid your hair while chemically relaxed? Do you hot comb your hair? Do you use a hot curler or hair rollers to curl your hair? Adapted from Callender et al. 16 diagnosis. (iii) Examination of the hair shafts is also helpful when evaluating the degree of hair breakage and weathering. Ancillary tests Fig 4. This woman with afro-textured hair presented with hair loss. Close examination reveals the presence of both traction alopecia (a) and central centrifugal cicatricial alopecia (b). Scalp examination should include three key steps. (i) Close inspection of the scalp: clues to help distinguish scarring from nonscarring hair loss include the presence or absence of follicular orifices, tufting and textural changes. Other useful clinical signs include perifollicular erythema, scaling, crusting, pustules, dyspigmentation and atrophy. Areas of alopecia should be quantified using validated instruments, including the Central Scalp Alopecia Photographic Scale 38 (Fig. 5) and the Marginal Traction Alopecia Severity Score 39 (Fig. 6). In the setting of severe alopecia, the grading scale developed by Olsen et al. for use in the setting of alopecia areata can also be used to document the extent and site of hair loss. 40 (ii) The pattern of alopecia should also be noted. A receding frontal hairline is characteristic of frontal fibrosing alopecia (FFA), but TA and alopecia areata (AA) should also be considered. The use of dermoscopy may help in this setting (see later discussion). Vertex scalp involvement may result from many causes, including CCCA, female pattern hair loss (FPHL), lichen planopilaris (LPP), chronic cutaneous lupus erythematosus (CCLE) and AA. Other clinical findings, ancillary tests (e.g. dermoscopy), and scalp biopsies can be used in this setting to confirm the These tests are useful adjuncts to routine history and clinical examination. Dermoscopy Dermoscopy is a fast, noninvasive and cheap technique, which can be used as an ancillary tool for diagnosing hair and scalp disorders To date, 1 2-mm pale dots, thought to represent fibrous tracts, have been reported on dermoscopic examination of the scalp of persons with afro-textured hair. 44 Although thought to be a sign of scarring (having been observed in both LPP and CCCA), these white dots have also been observed in the setting of nonscarring alopecia, such as AA and pattern hair loss. 45 Thus, some authors have postulated that these pale dots may represent the acrosyringium. 45 Further studies are required to better understand these dermoscopic findings. Another useful application of dermoscopy is in differentiating between FFA and AA (ophiasis/marginal). Yellow scalp dots are characteristic of the latter condition, while perifollicular scaling may be seen in LPP. 42 Hair pull test During the hair pull test, the quantity and quality of hairs pulled out are assessed. In the setting of telogen effluvium

6 24 Hair and scalp disorders in women of African descent, A. Salam et al. 0 (TE), for example, a higher number of telogen hairs will be pulled out (increased telogen count). 47 In acquired trichorrhexis nodosa, hairs are easily broken, appearing unequal in length. Nodes are also present, consisting of foci of frayed cortical fibres that bulge through a ruptured cuticle. On light microscopy, these nodes simulate two paint brushes whose bristles have been pushed together. 47 1A 1B Photography Photography is an essential tool in the clinical assessment of alopecia, especially for assessing disease progression, as well as response to therapy. Protocols should be standardized to enable comparisons of serial photographs over time. Investigations 2A 3A 4A 5A Fig 5. The Central Scalp Alopecia Photographic Scale in African- American women. Pattern 0, normal hair density, no hair loss; patterns 1 and 2, differential diagnosis includes early central centrifugal cicatricial alopecia (CCCA), female pattern hair loss, telogen effluvium (acute and chronic); patterns 3, 4 and 5, probable CCCA. Reprinted from Olsen et al., 38 with permission from Wiley- Blackwell. 2B 3B 4B 5B Other investigations to be considered include blood tests where indicated, swabs particularly from pustular lesions, and scalp scrapings when considering fungal scalp infections. 4 There is inconclusive evidence to support the use of multiple generic blood tests in the setting of alopecia. It is our opinion that the need for blood tests should be guided by the clinical findings. 4 Scalp biopsy is an invaluable ancillary tool for the assessment of alopecia; however, it must be performed properly to optimize outcomes. Selection of the site of biopsy is important. In the setting of scarring, the active border of the scarred region yields the best results (Fig. 7). Dermoscopy may aid in selecting the optimal biopsy site. 46 Under specific circumstances other biopsy sites may be chosen, e.g. areas of advanced disease in patients with FPHL to determine follicular density and thus likelihood of response to treatment. Fourmillimetre-sized punch biopsies 48 are preferable, and they should be deep enough to include subcutaneous tissue. This ensures that the entire follicular unit is studied. Once collected, the specimen may be sectioned horizontally and/or vertically (Fig. 8). Horizontal sections, developed by Headington in 1984, 49 have the advantage of ensuring a greater number of hair follicles are studied and hence focal pathology is not missed. The disadvantage of this approach is that it requires familiarity with scalp microanatomy in a different sectioning plane. 49 Vertical sections, on the other hand allow easy visualization of the dermal epidermal junction, although not all follicles can be studied. The best approach is to use protocols that combine both horizontal and vertical sections (Fig. 9), in association with good clinicopathological correlation. It is also important that the reporting pathologist/dermatopathologist is experienced in the interpretation of hair and scalp biopsies. The laboratory staff should also be trained in the specialist handling of these specimens. Common hair and scalp disorders A wide variety of hair and scalp disorders may occur in women of African descent, although some conditions appear to be specific to this cohort.

7 Hair and scalp disorders in women of African descent, A. Salam et al. 25 Fig 6. The Marginal Traction Alopecia Severity Score. Reprinted from Khumalo et al., 37 with permission from Wiley-Blackwell. Hair shaft abnormalities Acquired trichorrhexis nodosa This is due to excessive physical and chemical stresses on the hair shaft as a result of excessive brushing, combing, braiding, as well as heat, and chemical processing. 16,53 Hair-grooming products (e.g. spritzes, gels and hair sprays) can also contribute to the problem. Typically, patients complain of hair breakage with minimal manipulation of the hair shaft. Examination reveals breakage of the hair shafts at variable distances from the scalp. This can be demonstrated via the hair pull test, which reveals short hairs that lack roots, have paintbrush tips and fractures along the shaft. 47 The mainstay of treatment involves minimizing damaging hair care practices. There is some anecdotal evidence to suggest that biotin supplementation may help. 54 Both hypothyroidism 55 and zinc deficiency 56 are associated with this condition; therefore levels should be assessed, if clinically indicated, and supplementation instituted if appropriate. Pathological straightening of the hair shaft Straightening of the hair shaft, or losing the curliness of afrotextured hair occurs in patients with human immunodeficiency virus (HIV), often prior to the development of AIDS. 57,58 This phenomenon has also been reported in other conditions, e.g. chronic pancreatitis, liver disease, rheumatoid arthritis, as well as kwashiorkor in children. 59 Management consists of identification and treatment of the underlying associated condition.

8 26 Hair and scalp disorders in women of African descent, A. Salam et al. Fig 7. Selection of the biopsy site in a woman with central centrifugal cicatricial alopecia; biopsy of an active border (red circle) offers the best chance for determining the cause of the alopecia. If the centre of the scarred area is biopsied, the pathologist/dermatopathologist will only be able to confirm that there is scarring and not the cause of the scarring. Reprinted from Dadzie et al., 4 with permission from Wiley- Blackwell. (a) (b) Fig 8. A comparison of horizontal and vertical scalp sections. Vertical sections (a) enable the dermal epidermal junction to be better visualized; however, fewer follicles can be evaluated. In contrast, horizontal sections (b) enable the entire follicular unit to be assessed; thus, focal pathology can be identified. Reprinted from Dadzie et al., 4 with permission from Wiley-Blackwell. Scalp disorders Seborrhoeic dermatitis This is a chronic, relapsing, inflammatory condition that classically presents with itching, scaling and erythema of the scalp. This may be associated with a nonscarring alopecia secondary to TE. The association of seborrhoeic dermatitis Fig 9. A guide to taking the correct biopsies in the setting of nonscarring and scarring alopecia. H&E, haematoxylin and eosin; IMF, immunofluorescence. Reproduced from Stefanato et al., 50 with permission from Wiley-Blackwell. (especially severe and difficult to control disease) with HIV infection should be borne in mind. 60 Examination reveals diffuse, fine scaling of the scalp, which may involve other sites, e.g. forehead, eyebrows, nasolabial folds and ears. Hypopigmented and annular skin lesions may also be observed, as well as lichen simplex chronicus from chronic scratching. Histopathology shows the following epidermal changes: parakeratosis (including shoulder parakeratosis), in association with mild spongiosis and psoriasiform epidermal hyperplasia. There may be an associated mild inflammatory infiltrate within the dermis. There remains a lack of randomized controlled clinical studies evaluating the management of seborrhoeic dermatitis in women of African descent. Thus, current therapeutic strategies are based on anecdotal evidence. 16 They include avoidance of specific hair care products, such as hair gels, sprays and spritzes; and the use of antiseborrhoeic medicated shampoo. Agents such as zinc pyrithione are better because of their minimal drying effect on the hair shaft. Selenium sulfide and ketoconazole shampoo are also helpful in this setting. Patients should be advised to place the selected medicated shampoo directly on to the scalp, leaving it on for 5 10 min before washing off. Patients may then use their normal shampoo and conditioner. It is preferable to use these products once per week to minimize the drying effect on the hair (anecdotal experience of O.E.D.). If the disease is severe, topical corticosteroids or immune-modulatory drugs such as pimecrolimus may be used to treat the inflammatory component of the disease. 61 Psoriasis This presents as thick, scaly plaques of the scalp, that may be associated with alopecia ( psoriatic alopecia ) and/or other cutaneous features. The histopathological findings of psoriatic

9 Hair and scalp disorders in women of African descent, A. Salam et al. 27 alopecia have been reported to be both scarring and nonscarring in nature. Silva et al. 62 performed a retrospective analysis of 33 scalp biopsies from 31 patients with a histopathological diagnosis of scalp psoriasis. They reported the occurrence of alopecia as a presenting feature in 48% of cases. Histopathological features noted included scale crust with neutrophils, psoriasiform epidermal hyperplasia and hypogranulosis. They also observed infundibular dilatation (87%), perifollicular fibrosis (77%), perifollicular lymphocytic inflammation (68%), thinning of the follicular infundibulum (55%) and fibrous tracts (28%). They also noted that sebaceous glands were absent in 60% and atrophic in 25% of cases. 62 Management of scalp psoriasis in women of African descent is as per other races, with some suggested modifications. Medicated shampoos should be used (as described above for seborrhoeic dermatitis), with or without topical corticosteroids. The two-compound scalp formulation, calcipotriol/betamethasone dipropionate is also an option. 63 Tinea capitis Tinea capitis is infrequent in healthy adults, being generally a disease of childhood. If present in adults (especially inflammatory subtypes) then underlying immune suppression should be considered. 64 Periodic acid Schiff (PAS) stain to identify fungal spores and hyphae should be performed as part of the routine histological assessment of scalp biopsies. 65 and 7). The involved area appears smooth and shiny, with loss of follicular orifices. There may be scalp dysaesthesia and/or papules or pustules, as well as itching. This latter feature has been shown to correlate positively with disease severity, making it an important and sometimes early clinical finding. 75 The Central Scalp Alopecia Photographic Scale (Fig. 5) 38 can be used to assess the severity of disease. Histopathological findings (Figs 10 and 11) 47,65 include reduced number of terminal anagen follicles, with loss of sebaceous glands, concentric perifollicular fibrosis, compound follicles and eccentric follicular epithelial atrophy. The latter is due to marked thinning of the outer root sheath, with close approximation of the hair shaft and dermis (this culminates in naked hair shafts, associated with a foreign body giant cell reaction). The presence of premature desquamation of the inner root sheath is considered to be a specific diagnostic finding of CCCA by Sperling. 76 Other authors disagree and have demonstrated the presence of premature desquamation of the inner root sheath in other settings, e.g. LPP. 77 It has been suggested that staining for cytokeratin and cytokeratin correlates with premature desquamation of Scarring alopecias Central centrifugal cicatricial alopecia LoPresti et al. 66 first described this disorder as hot comb alopecia in 1968, owing to the initial incorrect association with the use of hot combs. Other names have also been used to describe this entity (chemically induced cosmetic alopecia by Nicholson et al. in 1993; 67 follicular degeneration syndrome; 68 central centrifugal scarring alopecia by Sperling et al. in 2000), 69 and finally the term central centrifugal cicatricial alopecia used by the North American Hair Research Society in This is classified as a lymphocytic primary scarring alopecia that predominantly affects, but is not exclusive to women of African descent. 70 The disease primarily affects the crown and/or vertex scalp regions, sparing the occiput. The aetiopathogenesis of CCCA remains unknown, although hair-grooming practices have been implicated. Recent data link this disease to the use of sewn-in weaves and artificial hair extensions. 22 There is also some evidence to suggest a genetic predisposition, with Dlova and Forder 71 recently reporting the occurrence of families with CCCA. Finally, there are limited data linking CCCA with type 2 diabetes mellitus. 31 This is especially pertinent given the emerging role of peroxisome proliferator-activator receptor (PPAR)-c in the aetiopathogenesis of scarring alopecias such as LPP. 72,73 Clinically, CCCA presents as a slow-growing area of alopecia involving the crown and/or vertex scalp regions 3,74 (Figs 4b Fig 10. Central centrifugal cicatricial alopecia (subisthmic area): hair follicles exhibiting premature desquamation of the inner root sheath and eccentric thinning of the follicular epithelium (haematoxylin and eosin stain; original magnification: 9100). Courtesy of Catherine M. Stefanato, St John s Institute of Dermatology, London, U.K. Reprinted from Dadzie et al. 4 with permission from Wiley-Blackwell. Fig 11. Central centrifugal cicatricial alopecia (suprabulbar region): naked hair shaft associated with a foreign body giant cell reaction (haematoxylin and eosin stain; original magnification: 9200).

10 28 Hair and scalp disorders in women of African descent, A. Salam et al. the inner root sheath. The direct immunofluorescence findings for CCCA have not been thoroughly evaluated. 47 There remains a lack of published randomized controlled studies evaluating therapeutic interventions for CCCA. Thus, current treatment algorithms are based on anecdotal evidence. It is important that goals of treatment are clearly stated at the start of any treatment regimen. This is often to halt progression of alopecia and stimulate hair regrowth from any remaining viable follicles. Firstly, minimization or stoppage of damaging hair care practices is advocated. Thus, patients should be counselled to stop or increase the frequency between the applications of chemical relaxers (e.g. from 8 to 12 weekly). Sewn-in weaves and tight braids should be avoided. Wigs can be used instead. Medical treatment should be initiated early, using a combination approach, consisting of a systemic anti-inflammatory agent (low-dose doxycycline or hydroxychloroquine), topical corticosteroids (e.g. Dermovate â ; GlaxoSmithKline, Uxbridge, U.K.) two to three times per week, 2 5% minoxidil, as well as monthly triamcinolone injections into the perilesional and alopecic areas. This regimen is normally continued for 6 months, after which response should be objectively evaluated before deciding on whether treatment should be continued for another 6 months. In advanced cases, it may be preferable not to offer any medical therapy in view of the poor prognosis. Psychological support at all stages of the disease process should be given. Patients should be given information about support groups running through organizations such as the Cicatricial Alopecia Research Foundation (CARF). Patients should also be counselled about camouflage techniques at all stages of the disease process. This includes the use of synthetic fibres, such as Nanogen â fibres (Nanogen, London, U.K.) and colourmatched make-up. Again information about these camouflage options can be obtained from organizations such as CARF. Finally, hair transplantation 16,80 can be offered. This should be done with caution due to the high risk of keloid formation in this cohort. Furthermore, the disease must be suppressed with appropriate medical therapies prior to undertaking hair transplantation, in order to minimize or prevent the chance of recurrence of the disease. Chronic cutaneous lupus erythematosus Fig 12. Extensive scarring alopecia secondary to chronic cutaneous lupus erythematosus. Reprinted from Dadzie et al., 4 with permission from Wiley-Blackwell. Fig 13. Chronic cutaneous lupus erythematosus: scanning magnification of a horizontally sectioned biopsy showing advanced loss of hair follicles and a perifollicular moderately dense lymphoid cell infiltrate with increased interstitial mucin. The infiltrate involves the eccrine glands, and also shows a perivascular and perineural arrangement (haematoxylin and eosin stain; original magnification: 940). Courtesy of Catherine M. Stefanato, St John s Institute of Dermatology, London, U.K. Reprinted from Dadzie et al., 4 with permission from Wiley-Blackwell. About one-third of cases of CCLE are associated with a scarring alopecia. 81 Clinically, there is an area of cicatrix with atrophy, telangiectasia and dyspigmentation (Fig. 12). Lesional histology 47,65 (Fig. 13) shows follicular drop-out with reduced number of terminal anagen follicles, loss of sebaceous glands, perifollicular fibrosis (advanced stages), as well as a superficial and deep perivascular and periadnexal inflammatory infiltrate (composed predominantly of lymphocytes, with admixed plasma cells). There is also follicular plugging and vacuolar interface changes affecting the follicles at the level of the infundibulum. Similar vacuolar interface changes may also involve the surface epithelium. Increased dermal mucin (highlighted by the use of special stains such as mucicarmine and/ or colloidal iron) and basement membrane thickening (highlighted with PAS stain) are also present. Clues to the histopathological diagnosis of CCLE include the presence of perieccrine and perineural (O.E.D., unpublished observation) inflammation. Direct immunofluorescence demonstrates the presence of multiple immune deposits (IgG, IgM, IgA and complements) along the dermoepidermal junction and follicular basement membrane. Management of CCLE includes topical and/or intralesional corticosteroids, as well as systemic agents such as antimalarials and oral retinoids. 82 Other therapeutic interventions include

11 Hair and scalp disorders in women of African descent, A. Salam et al. 29 topical immunomodulators, dapsone, methotrexate or mycophenolate mofetil. Lichen planopilaris and frontal fibrosing alopecia Both of these conditions are lymphocyte-mediated primary scarring alopecias, affecting both men and women, presenting either as multiple patches of scarring alopecia or a band-like symmetrical area of recession of the frontotemporal hair line (Fig. 14). 83,84 Perifollicular crusting and erythema may also occur. As with CCCA, itching is an important symptom that may correlate with disease activity. The lonely hair sign, 85 absence of the fringe sign (seen in TA) 86 and loss of eyebrows 85 are all important clinical clues for the diagnosis of FFA and exclusion of other differential diagnoses, e.g. TA. LPP may also present in a similar pattern to FPHL. 87 Although FFA was initially thought to affect mostly postmenopausal white women, several recent reports have demonstrated its presence in premenopausal women of African descent. 83,84 Histopathology 47,65 shows loss of terminal anagen follicles, increased number of fibrous tracts, loss of sebaceous glands, perifollicular fibrosis (advanced stages), as well as a lichenoid interface changes affecting the follicular epithelium (especially between the isthmus and infundibulum) (Fig. 15). In advanced cases, the infiltrate backs away from the follicle, which shows a myxoid perifollicular fibrosis. The infiltrate is located in the periadventitial dermis, distinguishing LPP from CCLE, in which there is spill over into the reticular dermis. There may or may not be an associated band-like lichenoid infiltrate involving the dermoepidermal junction. Direct immunofluorescence shows typically a shaggy or linear deposition of fibrinogen around the basement membrane zones of affected areas. Distinguishing the histopathological findings of late stages of CCCA and LPP may be difficult because of a shared common pathway for all end stage scarring alopecias. A link between LPP and the metabolic syndrome has been demonstrated through studies demonstrating the importance of PPAR-c in healthy pilosebaceous units, 72 and PPAR-c agonists have been successfully used to treat LPP. 73 The aetiology of FFA remains unknown. Various hypotheses exist including environmental and genetic factors. 88 The management of LPP and its variants includes the use of topical and intralesional corticosteroids, and/or oral systemic agents such as corticosteroids, hydroxychloroquine, doxycycline, mycophenolate mofetil and ciclosporin. 82 Folliculitis keloidalis nuchae FKN (Fig. 16) predominantly affects men rather than women of African descent and for this reason, our discussions will be brief. The characteristic clinical features are those of papules, pustules and/or keloids occurring primarily at the occipital scalp region. 89 These patients also typically have an associated scarring alopecia of the vertex scalp similar to folliculitis decalvans (O.E.D., unpublished observation). Recently, Khumalo Fig 14. Frontal fibrosing alopecia: a band-like symmetrical recession of the frontal hair line; there is also associated loss of the eyebrows. Reprinted from Miteva et al., 83 with permission from Wiley-Blackwell. (a) (b) Fig 15. Lichen planopilaris (isthmus): perifollicular lymphoid cell infiltrate with vacuolar interface changes and perifollicular fibrosis (haematoxylin and eosin stain; original magnification: 9200). Courtesy of Catherine M. Stefanato, St John s Institute of Dermatology, London, U.K. Reprinted from Dadzie et al., 4 with permission from Wiley-Blackwell. Fig 16. Folliculitis keloidalis nuchae in (a) a female and (b) a male patient.

12 30 Hair and scalp disorders in women of African descent, A. Salam et al. Nonscarring alopecias These will not be discussed in detail as there are no obvious ethnic/racial differences in presentation and management. There are, however, a few important aspects of diagnosis and management that should be highlighted: (i) there are a lack of published data pertaining to the epidemiological and clinical aspects of FPHL in women of African descent; (ii) distinguishing FPHL and CCCA in this cohort may be challenging when based solely on clinical findings, especially as they may coexist; and (iii) there is a risk (albeit small) of inducing vitiliginous leucoderma 93,94 when diphencyprone is used to treat AA in individuals with richly pigmented skin. Fig 17. Traction alopecia. et al. 90 have highlighted the possibility of a link between haircut-associated bleeding in this condition and HIV transmission, especially in countries (e.g. South Africa) with high rates of HIV infection. Discussion about the treatment of FKN is beyond the scope of this review. Biphasic alopecia Traction alopecia This is an important and common cause of alopecia in women of African descent. Early diagnosis is important as hair loss is reversible in the early stages, but over the course of months or years, scarring ensues (termed biphasic alopecia). Patients typically present with symmetrical frontotemporal hair loss (Figs 4a and 17) and/or occipital scalp hair loss. Closer inspection may reveal residual vellus hair follicles, 86 erythema or folliculitis. 91 Traction usually takes months/years to cause alopecia and is associated with hairstyles such as ponytails, tight braids, hair weaves, hair rollers or the wearing of tight headscarves. The risk of developing this condition increases with painful traction, and with traction-associated hairstyles on chemically relaxed hair. 21 Histopathological features 47,65 of early traction are similar (although more subtle) to those observed in trichotillomania. Features include increased number of non-anagen follicles, without significant inflammation, distorted hair follicle anatomy, trichomalacia, perifollicular and intrafollicular haemorrhage and melanin casts. In late stage TA, there is follicular dropout, with replacement of follicular units by fibrous tracts; however, sebaceous glands are generally preserved. This is a unique finding as most cases of scarring alopecia are associated with loss of sebaceous glands. Patient education regarding hair-grooming practices (e.g. avoiding tight, painful braids and braiding only natural, chemically untreated hair) is an important aspect of managing this condition. 16 Anecdotal evidence supports the use of topical/ intralesional corticosteroids, topical/oral antibiotics (in the setting of folliculitis), as well as 2% minoxidil. 92 Hair transplantation is also an option when scarring alopecia ensues. 80 Conclusions Hair and scalp disorders are a significant problem in women of African descent. Understanding the biology of afro-textured hair, as well as the hair-grooming practices of women of African descent is important when approaching the diagnosis and management of this cohort. Currently, most of the treatment strategies advocated for managing these disorders are based on anecdotal evidence. Thus, more research is required to enable better evidence-based treatments to be developed. 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