British Journal of Dermatology 2003; 148: 493500.

Clinical and Laboratory Investigations Skin diseases associated with the cosmetic use of bleaching products in women from Dakar, Senegal
A.MAHE, F.LY, G.AYMARD* AND J.M.DANGOU
` Department of Dermatology, Institut dHygiene Sociale, Dakar, Senegal ` *Department of Pharmacology, Groupe Hospitalier Pitie-Salpetriere, Paris, France Department of Pathology, Institut Pasteur, Dakar, Senegal Accepted for publication 8 September 2002

Summary

Background The cosmetic use of bleaching products is considered a common practice in darkskinned women from sub-Saharan Africa. However, there are few studies on this subject. Objectives To increase the knowledge about the dermatological consequences of this practice in Dakar, the capital of Senegal. Methods A representative sample of 368 adult women presenting at our dermatological centre was selected. Each woman was questioned about her cosmetic use of bleaching products. Next, the following data were recorded in 425 women who used bleaching products: names and types of products used; modalities of the skin bleaching practice; skin diseases motivating the dermatological visit, with recording of their clinical features; and results of a full skin examination. The active substances of the bleaching products were determined mainly by reading the indications on their packages; with products of unknown composition, a pharmacological analysis of samples was done. A statistical analysis was performed. Results Of the 368 women questioned, 194 (527%) were current users of bleaching products. Concerning the 425 users enrolled, products were applied on the whole body in 92% of users, with a median duration of use of 4 years. The active principles used included hydroquinone (used by 89% of users), glucocorticoids (70%), mercury iodide (10%) and caustic agents (17%); 13% of users used products of unknown composition. In the samples that were analysed, hydroquinone was found at concentrations of between 4% and 87%. Concerning steroids, superpotent (class 1) glucocorticoids predominated. The main skin complaints in bleaching products users included dermatophyte infections (n 105) and scabies (n 69), both often unusually extensive and severe; acne (n 42), often severe; eczema (n 41); irritant dermatitis (n 14); and dyschromia (n 26, including 14 cases of exogenous ochronosis). The skin examination noted features apparently disregarded by users: striae (noticed in 39% of users), and macular hyperchromia involving the face, mainly the periocular area (33%). The statistical analysis showed that glucocorticoid use was associated with the presence and severity of infectious skin diseases, and of acne. Conclusions More than half of the adult women presenting at our dermatology centre were using bleaching products. Most skin diseases observed in bleaching products users appeared to be induced, aggravated or modied by this practice. Superpotent topical glucocorticoids appeared to be the main agents responsible for the observed complications. The cosmetic use of bleaching products therefore has a major impact on our current dermatological practice. Key words: dermatophyte infections, glucocorticoids, hydroquinone, scabies, Senegal, skin bleaching products

Correspondence: A.Mahe, BP 16705, Dakar-Fann, Senegal. E-mail: mahe@refer.sn 2003 British Association of Dermatologists

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The cosmetic use of skin bleaching products is a common practice in dark-skinned women from subSaharan Africa.1 In Bamako, the capital of Mali, 25% of adult women reported current use of such products.2 In South Africa, the total sales volume of skin lighteners was estimated in 1986 at 30 million.3 Well-described complications of the practice are exogenous ochronosis related to long-term use of hydroquinone,4 and nephrotic syndromes secondary to mercury.5 Of more recent use, topical glucocorticoids are also potent lighteners.1,6 However, there are few studies on this important subject. In particular, there has been no satisfactory attempt to assess the whole range of the dermatological complications of the use of bleaching products. The aim of our study was therefore to increase the knowledge about the dermatological consequences of this practice in an African community, through the following objectives: to report contemporary modalities of cosmetic use of bleaching products; to describe a wide range of dermatological complications of that practice; and, nally, to evaluate its impact on the practice of dermatology in this environment.

products for cosmetic reasons, all women were included; the size of the sample (368) was calculated in order to measure a proportion of use of 40% (anticipated proportion obtained on a pretest sample), with an absolute precision of 5%, and a condence interval of 95% (n 1962 04 06 0052 368). Once this sample was completed, only women reporting present use of bleaching products were enrolled. The bleaching power of the products used as cosmetics was established through several channels: mainly, reading on the packages the mention of well-known active lightening substances (i.e. hydroquinone, steroids or mercury); or, when these data were not available, on an advertised bleaching activity, according to the statements of users and of the numerous local retailers of bleaching products. When credibly said to be used for a medical purpose, potentially lightening substances, such as steroids, were not considered to be used cosmetically. Data collection Questionnaire. In addition to the recording of general data (age, obstetric history), the following data were collected: (i) for women who reported present use of bleaching products, the names and types of products used during the last 3 months, the duration of the practice, frequency of application, areas of the body involved, quantities used monthly and their estimated costs, and attitude towards their use during pregnancy and lactation; (ii) for women who denied present use of bleaching products, any former use of these products. Skin examination. The skin disease(s) motivating the visit to our centre was (were) registered, with recording of clinical aspects. In addition, a full skin examination was performed in women using bleaching products. Most diagnoses were exclusively clinical, and were based on classical typical features of diseases;7 in only a minority of patients with non-diagnostic pictures were simple complementary investigations performed, e.g. direct microscopic examination of samples collected by sellotape for tinea versicolor, or skin biopsy in other cases. Pharmacological analysis. Samples of bleaching products of unknown composition that were commonly used were obtained (Niuma Extra Cream, Skin Light cream, Akagni cream, Sivoclair cream and milk, Top-tone cream and Peau Claire cream). Synthetic glucocorticoids (betamethasone, dexamethasone, clobetasol, hydrocortisone, desonide and uocinonide)

Patients and methods

Dakar, the capital of Senegal, has a population of about 2 million. Senegal is a sub-Saharan Sahelian country of 9.5 million inhabitants, with a gross national income per capita of US$490 (World Bank Atlas method, 2000). Located in the popular ward of Medina, our institution ` (Institut dHygiene Sociale, Dakar, Senegal) is one of the only two public centres in Dakar that specialize in dermatology. About 12 000 patients per annum of all ages and both sexes visit this centre with skin complaints. The cost for a dermatological visit is 500 Francs CFA (about 080 Euros). Most people visiting this centre belong to the lower and middle classes of Dakar. Inclusion criteria The population study was of women aged 16 years or more, presenting for a dermatological reason at our centre. Only new patients were considered. On 1 day per week during 1 year (2000 2001), each woman was questioned about her present cosmetic practices, focusing on the use of bleaching products; women who said that they had recently stopped their bleaching practice because of the skin problem for which they visited our centre were considered as present users. Our study was performed in two stages. First, to evaluate the proportion of women using bleaching

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and hydroquinone were assayed in samples by highperformance liquid chromatography with an ultraviolet visible diode array spectrophotometer. Full ultraviolet spectra were recorded and automatically compared with spectra stored in a library. A calibration curve was constructed for each assay by adding known amounts of each drug to drug-free cream. Each sample was assayed in triplicate, and nal results were given as mean of weight percentage (coefcient of variation percentage 100 SD mean). Statistical analysis Data were processed with EPI-INFO version 604. The v2 test, Fishers exact test and the KruskalWallis test were used to study the association of skin diseases with the use of certain bleaching products, or with the duration of the practice.

Results
In total, 599 women aged 1670 years (mean SD 31 114) were included. Of the representative sample of 368 women, 194 (527 5%) reported current cosmetic use of bleaching products. The duration of the practice varied from 1 month to 35 years (median 4 years). In addition, 37 more women (10%) reported previous use. Modalities of use of bleaching products The following data were collected in 425 users of bleaching products (194 from the representative sample, plus 231 included later). Products used. One hundred and seventeen different brands were recorded; those used most frequently are shown in Table 1. Eighty-ve women (20%) used only

one product, while the others used two or more (mean 27, range 17). The brands were classied according to their active substance where known, i.e. hydroquinone, glucocorticoids, mercury or caustic agents (Table 1). The pharmacological analysis found 004% clobetasol propionate in Niuma Extra Cream, and hydroquinone at concentrations of between 4% and 87% in the other products tested (range of coefcient of variation percentage 0852%), while the only concentration of hydroquinone mentioned, as shown on only a minority of packages, was 2%. Glucocorticoid-based products were class 1 steroids in 93% of cases. Caustic products were either applied directly to the skin, or used as a diluent for other products. The active substances were used either alone (hydroquinone alone, 90 women; steroids alone, 16 women), or more often in various combinations (hydroquinone + steroids, 62% of users). Certain packages mentioned the presence of other substances such as plant extracts, lemon, citric acid, carotene (presented as an antioxidant for hydroquinone) or (rarely) sunscreens. The brands were all bought in specialized non-medical shops, without any medical prescription. With the exception of certain steroid-based compounds having a pharmaceutical presentation (e.g. Dermovate), most brands had a purely cosmetic presentation with no or imprecise warnings about possible adverse effects and contraindications. According to the packaging, they had been manufactured in various regions of the world (Africa, Europe, North America, Middle East, etc.). Modalities of application. Products were applied once or twice daily to the whole body in 92% of users. One hundred and seventy-six women reported use of bleaching products at the time of conception; 81% carried on with their use during pregnancy (27% increased it during the last trimester), and 87% during

Table 1. Main products used by 425 users of lightening agents. Brands are classied according to their active substance when known, and for each active substance by decreasing frequency of use Active substance Hydroquinone No. of users (%) 378 (89%) Branded products (type of product) Skin Light (M, C, S), Niuma (M), Top-tone (C), Sivoclair (M, C), Fair White (M, C), Peau Claire (M, C), MGC (M), Akagni (C, M), Immediat Clair (M, C), Clairliss (M), Black Star (M), HT 26a (M), CBLa (M), Body Clear (M, C), Emos (C) ` Tenovateb (C, G), Neoprosonec,d (G), Niuma Extra Cream (C), Movateb (C), PCb (C, G), Lumiereb (C), Neomatb,d (C, G), Topgeld (G), Dermovateb (C, G), Clovateb (C), Maximc (G), Prosonec (G), Dianab (C), Civicb (C, G), Fashion Fairb (C) Niuma (S), Rico (S), Sukisa Bango (S), Idole (S), Jaribu (S), Movate (S) Liquid soaps, hydrogen peroxide, salicylic preparations (1030% in vaseline, Sivoderm) Si Claire (M, C), Shirley (C), Asepso (S), Ideal (C)

Glucocorticoids

297 (70%)

Mercury saltse Caustic agents Unknown

43 (10%) 72 (17%) 55 (13%)

M, milk; C, cream; S, soap; G, gel. According to package labels: acontains 05% salicylic acid added to hydroquinone; bcontains 005% clobetasol propionate; ccontains 005% betamethasone dipropionate; dcontains neomycin sulphate; e13% mercury iodide. 2003 British Association of Dermatologists, British Journal of Dermatology, 148, 493500

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Table 2. Skin diseases recorded in 425 women using bleaching products Skin diseases motivating visits Mycoses Dermatophyte infection Candidiasis and nonspecic intertrigo Tinea versicolor Scabies Bacterial skin infections Other infectious diseases Acne Perioral dermatitis Eczema Irritant dermatitis Xerosis ichthyosis Isolated itching Dyschromia Hyperchromic Hypochromic Exogenous ochronosis Pigmenting keratosis pilaris Striae Poikilodermac Blue eard Facial hypertrichosis Others
a

Dermatoses nonmotivating visits found by systematic examination 23 6 8 81 2 16b 4 146 14 12 3 167 23 25 43 12

Total (percentage of all users) 128 (30%) 23 4 69 22 11 123 (29%) 2 43 14 22 15 154 (36%) 18 26 6 169 (40%) 24 25 43 92

105 17 4 69 14a 11 42 2 41 14 6 11 8 4 14 3 2 1 80

Including cellulitis (six cases) and disseminated folliculitis (ve cases); blocated on anterior legs; cpoikilodermatous appearance at the base of the neck; dbluegrey discoloration of external ears.

lactation. The quantity used was from one to four tubes per month for each type of product. The mean monthly quantity of steroids used was 95 g (range 15350). The estimated monthly cost of bleaching products varied from 250 to 25 000 Francs CFA (mean 3300 Francs CFA, i.e. about 5 Euros, to be compared with a monthly guaranteed minimum wage of about 70 Euros). Dermatological data The 448 skin diseases that motivated the visits to our centre in the 425 users of bleaching products are shown in Table 2. Unusual features were noticed in 75% of women with dermatophyte infections (such as widespread lesions, inammatory and or pustular features, involvement outside of skin folds noticeably in the face, resistance to usual treatments; Fig. 1); in 58% of women with scabies (widespread lesions, prominent hyperchromic burrows, crusted lesions; Fig. 2); and in three of the four women with tinea versicolor (location at the inner thigh, with deep depigmentation associated with supercial atrophy; Fig. 3). Acne followed the beginning of bleaching product use in 50% of patients, and was seriously inammatory in 29% of cases (Fig. 4).

Concerning eczema, the main sites involved were the face and neck, hands and feet, and inguinal and axillary folds. There was a chronology suggesting causality of a bleaching product in nine cases. Five cases of facial lupus-like photodistributed papular eruption, involving noticeably the malar areas, were observed (Fig. 5). No general features of lupus erythematosus were present. Histopathology performed in three patients showed lupus-like and or lichenoid features. The three patients who could be followed experienced rapid resolution of active papular lesions after stopping the practice together with local steroid therapy, with only persistent postlesional hyperchromia. In addition to the spontaneous complaints, a full skin examination of bleaching products users noted other skin features (Table 2). Striae were often widespread, atrophic or pigmented (Fig. 6). The 146 macular hyperchromias recorded mainly involved the face, noticeably the periocular area (124 cases; Fig. 7). Correlation of dermatoses with specic modalities of practice The statistical analysis concerned only the 425 bleaching products users, and skin diseases were grouped together irrespective of the presenting complaint.

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Figure 1. Widespread inammatory tinea corporis.

Figure 2. Disseminated lesions (including multiple pigmenting burrows) in a patient with scabies.

Steroid use was signicantly associated with the presence of dermatophyte infection, scabies, pyoderma, acne and striae, and with the severity of dermatophyte infection, scabies and acne (P < 005 in all cases). Steroid use was also associated with a lower frequency of eczema (P < 001). Hydroquinone was used by all patients with exogenous ochronosis, by those with a lupus-like eruption, and by eight of nine of the women with eczema with a chronology suggesting causality. Ochronosis, poikiloderma of the neck, periocular hyperchromia and a blue discoloration of the external ears were observed in women who had used bleaching products for a longer time (P < 001 in all cases).

Discussion
Two main criticisms can be made of our study. First, the dermatological diagnoses were based mainly on clinical grounds; this reects the dermatological practice in most tropical countries, where clinical accuracy

for the diagnosis of common dermatoses appears good.7 Moreover, the unusual features that we observed mainly showed an exaggerated pattern, rather than a really atypical one, therefore making the diagnosis easier. It is, however, possible that we ignored certain inconspicuous diseases for which special investigations would have been necessary, such as hair or nail mycosis. Second, several data were recorded through a questionnaire; there might be a reluctance by some women to answer questions about skin bleaching, an ofcially discouraged practice in many African countries.2 This may account for an underestimation in our evaluation of the frequency of the practice. In a representative sample of adult women visiting our dermatological centre, 527% were using bleaching products for a cosmetic purpose. This can be compared with prevalence studies conducted in Bamako (general population-based study)2 and in Dakar (hospital-based study),6 which found the use of bleaching products in

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Figure 3. Achromic tinea versicolor of the inner thigh.

Figure 5. Lupus-like eruption of the malar areas and forehead.

Figure 4. Acne seriously aggravated by corticosteroid use.

Figure 6. Prominent striae in a user of superpotent glucocorticoids.

about 25% of adult women. Because of the frequency of skin diseases in users of bleaching products,2,6 our gure of 53% of women using bleaching products in a dermatological centre appears reasonable.

Considering the substances used, there was a lack of accuracy in our data, because the true composition of the products can differ from the indications guring on the packages.8 Hydroquinone and glucocorticoid-based

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Figure 7. Periocular berloque dermatitis-like hyperpigmentation.

products predominated. In comparison with older reports, the high use of superpotent glucocorticoids reported here is striking.9,10 In addition, certain modalities of the use of bleaching products might facilitate complications: applying hydroquinone without sun protection; application to the whole body; and large quantities of class 1 steroids applied, with possible systemic absorption.11,12 Of particular concern was the fact that most women who used bleaching products when they became pregnant went on with their practice. This practice, attributed to a wish for clear skin at the ceremony of baptism, seems particularly hazardous.13 Despite patent protection and regulation of sales of compounds such as steroids, all brands were easily available in non-pharmaceutical shops, without seeing a doctor. The fact that some products in the same branded cosmetic range contained several distinct active ingredients, might also facilitate adverse effects. Concerning the skin diseases motivating the visits to our centre in women using bleaching products, classical complications of that practice, i.e. pigmentation disorders or caustic effects, appeared rarer than formerly.3,9 Instead, the most common diseases were infections, representing about half of the ailments (49%): such a high gure should be considered as exaggerated for an adult population, even in a tropical context.14 Dramatic features were common. As suggested by the statistical analysis, the frequency and or severity of infectious diseases appeared related to the use of topical steroids, as were many cases of acne. Concerning other dermatoses, a direct relationship with bleaching products use was not always so clear.

Eczema is a common disease at our centre, even in non-users of bleaching products. Actually this condition was comparatively less frequent in users of steroids. Nevertheless, certain cases, involving folds or sun-exposed areas, appeared chronologically related to the use of bleaching products, especially hydroquinone. More unusual were the ve cases of lupus-like eruptions involving the face. Similar cases were rst described in Senegal by Marchand et al.;9 it is not clear whether these were induced by photosensitizers such as hydroquinone. Finally, only a minority of skin diseases in bleaching products users appeared to have no link with bleaching products; in some of these cases, however, the presentation was made atypical by the application of bleaching products. The complete skin examination of women using bleaching products revealed several additional features, e.g. a photodistributed periocular berloque dermatitislike pigmentation, prominent striae and acne. The apparent disregard of these features by the bleaching products users was striking.2 In conclusion, the cosmetic use of bleaching products had a huge impact on our dermatological practice. More than half of adult women presenting at our centre were using such products. Most skin diseases diagnosed in bleaching products users appeared to be inuenced by those products: if we include clearly induced or aggravated cases of infectious diseases, acne, dyschromia, irritant or allergic dermatitis, as of more unusual diseases, at least 55% of the skin diseases motivating a visit in bleaching products users could be classied as complications of that practice; and if we include cases for which an eventual role of bleaching products is possible, this gure reaches 75%. This can be compared with a 1976 report from the same city, where the proportion of dermatological visits in women related to complications of the use of bleaching products was estimated to be only 2% of the total.9 Topical steroids have emerged in recent years as major lighteners, due to their potent bleaching power, and perhaps also their anti-inammatory activity that could limit the risks for dermatitis; nevertheless, they appeared here as the main agent responsible for the complications observed. Our experience in a nonselective dermatological centre in a big African city reects a pattern that is probably valid in other areas of sub-Saharan Africa. Health providers in other African cities, as well as those dealing with immigrant communities in northern countries, should be aware of this growing problem.

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