Medical and Environmental Risk Factors for the Development of Central Centrifugal Cicatricial Alopecia a Population Study

STUDY

ONLINE FIRST Medical and Environmental Risk Factors for the Development of Central Centrifugal Cicatricial Alopecia A Population Study

Angela Kyei, MD, MPH; Wilma Fowler Bergfeld, MD; Melissa Piliang, MD; Pamela Summers, MD

Objective: To investigate medical and environmental lished central scalp alopecia photographic scale, a score risk factors for central centrifugal cicatricial alopecia consistent with clinically evident central hair loss. Ad- (CCCA), the most common type of scarring alopecia in vanced central hair loss with clinical signs of scarring African American women. (grade Ն3) was seen in 59% of these respondents and was interpreted as clinically consistent with CCCA. Dia- Design: A population study involving a quantitative betes mellitus type 2 was significantly higher in those with cross-sectional survey of risk factors for CCCA. Survey CCCA (P=.01), as were bacterial scalp infections (P=.045) results are then correlated with a clinical evaluation for CCCA using a standardized, previously published cen- and hair styles associated with traction (eg, from braids tral scalp alopecia photographic scale. and weaves) (P=.02). Conclusions: Our survey results suggest that there is a Setting: Two African American churches and a health high prevalence of central hair loss among African Ameri- fair for African American women in Cleveland, Ohio. can women. Hair styles causing traction as well as in- Participants: A total of 326 African American women flammation in the form of bacterial infection may be con- who participated in the hair study. tributing to the development of CCCA. The increase in diabetes mellitus type 2 among those with CCCA is in Main Outcome Measures: Prevalence of CCCA in the line with the recent theory that cicatricial alopecia may general African American population and risk factors as- be a manifestation of metabolic dysregulation. sociated with CCCA. Arch Dermatol. Results: Of the 326 responders, 28% received a grade Published online April 11, 2011. of 2 or higher using a standardized, previously pub- doi:10.1001/archdermatol.2011.66

ENTRAL CENTRIFUGAL CICA- Most of the prevalence data on this en- tricial alopecia (CCCA) is tity come from Khumalo et al,6,7 who have a term coined by the conducted population studies in Africa North American Hair Re- looking at hairdressing and the preva- search Society (NAHRS) lence of scalp diseases commonly seen in toC describe a scarring hair loss, centered black children and adults. They found a on the vertex of the scalp, that spreads pe- surprisingly low prevalence of CCCA ripherally. It is almost exclusively used to (1.9%) in adults, most of whom were older describe this type of hair loss in African than 50 years, and no CCCA in children, American women and replaces previ- a surprising finding given that the com- ously used terms such as hot comb alope- mon hair grooming practices, such as cia, coined by Lopresti et al1 in 1968 and chemical relaxer use and braids linked to follicular degeneration syndrome, coined CCCA in African American women, are by Sperling and Sau2 in 1992. It is thought also used in this African population. In to be the most common pattern of scar- contrast, African American women in the ring hair loss seen in African American United States commonly present with this women, yet so little is known about its true entity, but true prevalence data in this Author Affiliations: Institute of prevalence among them. Moreover, the eti- population are lacking. 1 Dermatology and Plastic ology and risk factors, including environ- Lopresti et al were the first to pro- Surgery, Cleveland Clinic, mental, medical, and genetic risk factors, pose an environmental risk factor, namely, Cleveland, Ohio. remain to be elucidated.1-5 the use of hot combs in combination with

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©2011 American Medical Association. All rights reserved. autoimmune conditions, such as thyroid disease and DM; and Table 1. Central Hair Loss Grades (CHLGs) at Examinationa questions about hormonally driven conditions, such as unwanted and excessive hair growth, acne, and difficulty con- Respondents, ceiving (eTable, http://www.archdermatol.com) Finally, data Physician-assigned No. (%) of Total about methods of hair grooming, such as the age at which chemi- CHLGs Population Mean Age, y cal relaxers were first used and use of braids and weaves, were 0-1 224 (72) 40 compiled and analyzed to determine if there was any associa- 4,5 2-5 86 (28) 53 tion with CCCA. 3-5 52 (17) 58 The questionnaire was followed by a scalp examination using the standardized central scalp alopecia photographic scale to a Grades: 0, no central scalp hair loss; 1, minimal central scalp loss; grade hair loss (previously published by Olsen et al4). Using 2, clinically evident central scalp hair loss; 3-5, advanced central scalp hair this scale, Olsen et al4 interpreted a central hair loss grade loss. (CHLG) of 0 as normal hair; a CHLG of 1 to 2 as possibly early CCCA, androgenetic alopecia, or telogen effluvium; and a CHLG of 3 to 5 as probable CCCA given the usual characteristics of scalp oil to straighten the naturally curly African hair in scarring such as a shiny scalp and loss of follicular ostia found order to increase manageability. Since then, most other in this group. The scalp examination was conducted by der- forms of hair grooming methods used by African Ameri- matologists well trained in the area of hair loss, assessing for cans, including the use of braids, weaves, and chemical the characteristics of scarring. Standardized photographs of par- relaxers, have been linked to the development of CCCA. ticipants’ central scalp and anterotemporal scalp were ob- Gathers and Lim8 found an association between CCCA tained using professional photography. Validation of the CHLGs and hair weaves and braids but not relaxers. Khumalo assigned by each evaluator was ensured through a follow-up 6,7 group review of the scalp photographs. Answers to the ques- et al, however, reported 5 cases of acute chemical re- tionnaire were compared with the CHLG to determine if there laxer–associated scarring hair loss in African women. Bu- was a relationship between the development of CCCA and these 9 lengo-Ransby and Bergfeld also reported a case of chemi- various risk factors. The data were analyzed using frequencies cal relaxer–associated scarring hair loss. There are other and percentages. Spearman correlation was used for associa- reports of relaxers causing clinically significant chemi- tions; t tests, ␹2 tests, and Fisher exact test were used when cal burns and hair loss, but it is unclear if those affected appropriate. went on to develop CCCA. Thus, it is still uncertain 6-10 whether hair grooming practices are a risk factor. RESULTS While several studies have addressed environmental risk factors by examining hair grooming practices, few DEMOGRAPHIC DATA AND CLINICAL FINDINGS have addressed medical and genetic risk factors for this disorder. Given that CCCA has a distinct clinical pre- There were 326 African American responders, with a mean sentation and seems to predominantly affect African age of 50 years (Table 1). From the 326 responders, 16 Americans, it is important to ask whether risk factors were excluded from analysis because of a history of alo- unique to this population might contribute to the patho- pecia areata, lupus, and/or other hair loss pattern that was genesis of this disorder. Could CCCA be linked to other consistent with either of these types of hair loss. The common medical conditions found in African Ameri- NAHRS central hair loss scale was used to grade central cans, such as diabetes mellitus (DM), and other autoim- hair loss in all responders. A CHLG of 0 was interpreted mune conditions, such as lupus? Could it be linked to as normal central hair density without obvious hair loss. common skin conditions found in this population, such A CHLG of 1 was interpreted as minimal central hair loss as hypertrophic scars and keloids, fungal and bacterial and thus unlikely to have CCCA; a CHLG of 2 was in- scalp infections, and seborrheic dermatitis? Is there a fam- terpreted as clinically evident central hair loss and pos- ily history of this type of hair loss in patients with CCCA? sibly early evolving CCCA, although a diagnosis of an- These are important questions that remain unanswered. drogenetic alopecia must be entertained. A CHLG of 3 Given the lack of epidemiologic data, the main goal of to 5 was interpreted to be consistent with clinically evi- this study was to elucidate environmental as well as medi- dent CCCA (Figure 1 and Figure 2). A total of 86 of cal risk factors that may be associated with CCCA as well 310 respondents (28%) received a CHLG of 2 or higher as to estimate the prevalence of this disorder in African using this scale, a score consistent with clinically evi- Americans. dent central hair loss. Central centrifugal cicatricial alopecia (CHLGs 3-5) was seen in 59% of these respon- METHODS dents (Table 1).

This study, which was approved by the Cleveland Clinic’s SYSTEMIC METABOLIC DISEASE (Cleveland, Ohio) institutional review board, involved the administration of a questionnaire about risk factors for CCCA There was a low prevalence of type 2 DM in this popu- to 326 African American women at 2 churches and a health lation (8%) but a statistically significant increase (P =.01) fair for African American women at the Cleveland Clinic. The questionnaire consisted of questions about demographic data, in the prevalence of type 2 DM was observed in those such as age and participants’ level of education; questions with CCCA (CHLGs 3-5) when comparing those with about genetic susceptibility, such as family history of male- no CCCA (CHLGs 0-1). Type 2 DM was defined in the and female-pattern hair loss; questions about medical history, questionnaire as requiring diet modification or medica- such as personal history of bacterial, and fungal infections, tion for control. Data on weight or body mass index, which

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Figure 1. Early central hair loss (CHL). A, Grade 2A CHL represents widening of the central part with significant involvement of the frontal scalp. Differential diagnosis includes early central centrifugal cicatricial alopecia (CCCA) vs androgenetic alopecia. The letter “A” designates more involvement of the frontal scalp. B, Grade 2B CHL represents widening of the central part with preservation of the frontal scalp. Differential diagnosis includes early CCCA vs androgenetic alopecia. The letter “B” designates some sparing of the frontal scalp.

A B C

Figure 2. Advanced central hair loss (CHL). A, Grade 3A CHL represents advanced central hair loss and likely central centrifugal cicatricial alopecia (CCCA). The letter “A” designates more involvement of the frontal scalp. B, Grade 4B CHL represents advanced central hair loss and likely CCCA. The letter “B” designates some sparing of the frontal scalp. C, Grade 5A CHL represents advanced central hair loss and likely CCCA. The letter “A” designates more involvement of the frontal scalp.

is highly correlated with type 2 DM and also a large is- INFECTION sue among African American women, were not col- lected. Only 9% of the study population reported thy- There was a low prevalence of bacterial skin infections roid abnormalities. Most of them (74%) were classified (11.4%), but there was a statistically significant in- as having minimal central hair loss (CHLGs 0-1); how- crease in bacterial skin infections in those with CCCA ever, there was no statistically significant difference when compared with those without CCCA. There was no such this group is compared with those with advanced CCCA trend with fungal infections of the scalp, ringworm, or (P =.99) (Table 2 and Figure 3). vaginal yeast infections (Table 2 and Figure 4).

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16 Prevalence Prevalence by CHLG in Study 12 Diseases Population 0-1 2 3-5 Metabolic disease 8 Diabetes mellitus type 2 8.0 5.7 8.1 17.6 Thyroid disease 9.4 8.8 8.1 7.8

Patients With Type 2 DM, % Patients With Type 4 Infections Bacterial skin infection 11.4 9.7 10.8 19.6 0 Tinea corporis 10.5 11.0 10.8 7.8 0, 1 2 2, 3, 4, 5 3, 4, 5 Tinea capitis 11.4 10.1 16.2 13.7 Central Hair Loss Grade Vaginal yeast infections 48.2 49.8 48.6 41.2 Hormonal dysregulation Acne 69.0 68.7 67.6 72.5 Figure 3. Systemic disease. Type 2 diabetes mellitus (DM) Hirsutism, facial hair 52.0 52.4 59.5 43.1 disproportionately affects those with severe central centrifugal cicatricial alopecia (P=.01). Hair grooming Chemical relaxer 91.0 90.0 86.5 96.1 Braids, extentions, or weaves 47.6 48.0 32.0 57.0 Hot comb 44.0 42.0 46.0 49.0 20 Scar formation/keloid 6.0 4.0 21.6 3.9 Dermatitis 16 Seborrheic dermatitis, scaling 24.4 24.2 21.6 27.5 on the scalp Eczema, atopic dermatitis 13.3 15.4 13.5 3.9 12 Contact dermatitis From shampoos 0 8 From conditioners 0 From chemical relaxers 9.0 7.9 10.8 11.8 4 Patients With Bacterial Infection, % Abbreviation: CHLG, central hair loss grade. a 0 Data are given as percentages. 0, 1 2 2, 3, 4, 5 3, 4, 5 Central Hair Loss Grade HORMONAL DYSREGULATION Figure 4. Bacterial infection. Fisher exact test showed a statistically significant increase in bacterial skin infections in those with severe central There was also an increased rate of adult acne and diffi- centrifugal cicatricial alopecia (CCCA) compared with those without CCCA culty conceiving in those with CCCA (CHLGs 3-5) com- (P=.045). pared with those without CCCA (CHLGs 0-1), but this was not statistically significant (data not shown) (Table 2). Table 3. Age of First Hair Relaxer Use and Onset HAIR GROOMING of Central Hair Loss

Of the 310 respondents, 286 (91%) relaxed their hair by CHLG 0-2 CHLG 3-5 chemical means. All participants began using chemical Patients, Age, Patients, Age, relaxer at an early age: 10.3 years on average for those Time Point No. Mean, y No. Mean, y with a CHLG of 0 to 2, and 13.0 years on average for those At first hair relaxer use 236 10.3 49 13.0 with a CHLG of 3 to 5. Also, all participants had onset When first hair 122 44.9 51 45.5 of hair loss at a later age, with average ages of 44.9 years loss noticed for those with a CHLG of 0 to 2 and 45.5 for those with a CHLG of 3 to 5 (Table 3 and Figure 5). Ninety-four Abbreviation: CHLG, central hair loss grade. percent of those with clinically evident central hair loss (CHLG Ն2) had a history of chemical relaxer use. There cant (P =.02) increase in the use of traction hair styles was no statistically significant difference (P =.39) in the (braids, weaves) in those with CCCA compared with those use of chemical relaxer in those without central hair loss with less severe central hair loss (CHLG 2). (CHLGs 0-1) and those with clinically significant central hair loss (CHLGs 3-5). FAMILY HISTORY OF HAIR LOSS There was an overrepresentation of use of hot comb and traction hair styles in those with clinically evident central Participants were asked to estimate central hair loss in hair loss (CHLG Ն2) compared with those with minimal their male relatives using the Norwood pictorial male- to no central hair loss (CHLGs 0-1). There was no statis- pattern baldness scale. Males relatives included partici- tically significant difference (P =.35) in the use of hot comb pants’ fathers and maternal and paternal grandfathers. in those without central hair loss (CHLGs 0-1) and those They were also asked to grade central hair loss in their with CCCA (CHLGs 3-5). There was a statistically signifi- female relatives using the central hair loss scale devel-

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©2011 American Medical Association. All rights reserved. oped by Olsen et al.4 Female relatives included participants’ mothers and maternal and paternal grandmoth- A 50 ers. There was a statistically significant increase in central hair loss of the participant’s maternal grandfather among 47 those who had CCCA (CHLGs 3-5) (data not shown). 44 SCAR FORMATION AND CCCA 41 Given the increase in keloid formation among African Americans and the fact that CCCA is a scarring disor- 38 Patients Who Use Hot Comb, % der, participants were asked about their history of thick 35 scars (keloids). Looking at this variable, only 6% of par- 0, 1 2 2, 3, 4, 5 3, 4, 5 ticipants reported a history of thick scars, and it was not significantly increased in those with CCCA (CHLGs 3-5) (data not shown). B 60

DERMATITIS AND CCCA 48

Participants were asked about their history of seborrheic 36 dermatitis (scaling on the scalp) and eczema (atopic dermatitis) as well as the development of contact dermatitis 24 from chemical relaxers, shampoos, and conditioners. All groups, regardless of CHLG, reported high incidence of seb- 12 orrheic dermatitis (24% of total participants). This also held % Patients With Braids or Weaves, 0 true for dermatitis from relaxer use (9%), which was highly 0, 1 2 2, 3, 4, 5 3, 4, 5 reported in all groups. Eczema was reported by 13% of the participants and seemed to be inversely related to CCCA with most having little or no hair loss (Table 2). C 100

96 COMMENT

92 Central centrifugal cicatricial alopecia is the most common pattern of scarring hair loss seen in African American wom- 88 en, yet so little is known about the etiology and risk factors associated with this condition. Furthermore, the historical 84 association of CCCA with hot comb use is weak at best given Patients Who Use Relaxers, % the fact that there have been few epidemiological studies to 80 back this claim. In conducting this study, the main goal was 0, 1 2 2, 3, 4, 5 3, 4, 5 to elucidate environmental as well as medical and genetic Central Hair Loss Grade risk factors that may be associated with CCCA as well as estimate the prevalence of this disorder. Figure 5. Hair grooming. A, There is a trend toward increased hot comb use in those with the most severe central centrifugal cicatricial alopecia (CCCA), The results of this study suggest that hair grooming but this was not statistically significant (P=.35). B, There was increased practices that cause traction, such as weaves and braids, relaxer use in those with the most severe CCCA, but this was not statistically may be contributing to the development of CCCA be- significant (P=.39). C, Braids and weaves were associated with severe CCCA cause these styles are more commonly used in those with (P=.02). the most severe central hair loss to increase hairstyle ver- satility while camouflaging hair loss (Table 2 and CCCA.11,12 The fact that most African Americans use Figure 5B). This has some clinical bearing because trac- chemical relaxers in combination with braiding and tion can clinically produce folliculitis of the scalp, which other hair grooming practices makes it even more dif- can cause scarring if this inflammation is prolonged. Given ficult to tease out a relationship. Moreover, it is diffi- the fact that many African American women pay hun- cult to find a chemical relaxer–naı¨ve comparison dreds of dollars to have their hair braided and weaved, group because of the early age at which African Ameri- they often maintain these hair styles for weeks to months can children have their hair chemically relaxed and at a time to justify the money spent. The resulting pro- braided (Table 3). A younger population, however, longed traction can produce chronic folliculitis, which would still be legitimate as a comparison group can eventually lead to scarring. because presumably they have had fewer years of The relationship between chemical relaxer use and exposure than their adult counterparts. Overall, we the development of CCCA continues to be murky. feel that it is not unreasonable to assume that the scalp While it is clear that chemical relaxers weaken the hair may absorb some of the caustic chemicals found in shaft, which can result in increased breakage, it is relaxers and in time lead to damage of the scalp in the unclear whether it is related to the development of form of scarring.

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©2011 American Medical Association. All rights reserved. Our study also demonstrates that inflammation in the Financial Disclosure: None reported. form of bacterial infection and acne may also be contrib- Funding/Support: This study was supported in part by uting to the development of CCCA, a finding consistent the NAHRS and Proctor & Gamble. with the histopathologic characteristics of this disease, Role of the Sponsors: The sponsors had no role in the which show a lymphocytic perifollicular infiltrate in its design and conduct of the study; in the collection, analy- early stages. The fact that fungal scalp infection was not sis, and interpretation of data; or in the preparation, re- associated with CCCA was surprising given how prone view, or approval of the manuscript. this population is to fungal infection.13 Online-Only Material: The eTable is available at http: One of the most surprising findings of our data was the //www.archdermatol.com. overrepresentation of type 2 DM in those with CCCA. This Additional Information: The coinvestigators of this mul- group demonstrated that peroxisone proliferator of activated ticenter study are as follows: Dr Bergfeld, Cleveland Clinic; t-cell receptor gamma (PPAR-gamma), a transcription fac- Elise Olsen, MD; Duke University; David Whiting, MD, tor important in lipid metabolism by sebaceous glands was Baylor Hair Research and Treatment Center; Janet aberrant in the hair follicles of patients with the scarring hair Roberts, MD, Northwest Cutaneous Research Special- disorder, lichen planopilaris.14-16 These are important data ists; Faith Durden, MD, Case Western Reserve Univer- that need further study because CCCA may be a marker of sity; Leonard Sperling, MD, US Uniform Health Ser- metabolic dysfunction and, when present, can prompt cli- vices; Valerie Callendar, MD, Howard University College nicians to do further testing for DM in those affected. of Medicine; and Amy McMichael, MD, Wake Forest On the one hand, genetics may play a role, as is dem- University. A complete list of people from the Cleve- onstrated by the fact that a history of male-pattern bald- land Clinic site who agreed to participate in the study ness in the maternal grandfather was found to be a risk fac- and responded to the questionnaire was recently pub- tor for CCCA. On the other hand, hormonal dysregulation lished in the Journal of the American Academy of Derma- was not a risk factor. This study has raised many interest- tology (2011;64[2]:245-252). ing questions about the risk factors for CCCA, and fur- Additional Contributions: Jim Bena, BA, from the Cleve- ther studies are needed to explore these associations. land Clinic Department of Biostatistics and Epidemiology This study has several limitations. Because this is a sur- assisted with the statistical analysis portion of this study. vey, self-report bias must be considered. 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