Clinics in Dermatology (2010) 28, 140145

Tinea versicolor, tinea nigra, white piedra, and black piedra

Alexandro Bonifaz, MB, MSc a,, Fernando Gmez-Daza, BL, MSc b , Vanessa Paredes, MD a , Rosa Mara Ponce, MD a
Dermatology Service and Mycology Department, General Hospital of Mexico DO, Dr. Balmis 148, Colonia Doctores Mxico DF, 06720, Mexico b Dermatology Postgraduate Section, University of Carabobo, Valencia, Venezuela
a

Abstract Superficial mycoses are fungal infections limited to the stratum corneum and its adnexal structures. The most frequent types are dermatophytoses or tineas. Tinea versicolor involves the skin in the form of hypochromic or hyperchromic plaques, and tinea nigra affects the skin of the palms with dark plaques. White piedra and black piedra are parasitic infections of scalp hairs in the form of concretions caused by fungal growth. Diagnosis of these mycoses is made from mycologic studies, direct examination, stains, and isolation, and identification of the fungi. Treatment includes systemic antifungals, topical antifungals, and keratolytics. 2010 Elsevier Inc. All rights reserved.

Introduction
Superficial mycoses are fungal infections of the skin and its adnexal structures (hairs and nails) that invade solely the stratum corneum and the most superficial layers of the skin, causing minimal to no inflammatory reaction. The most frequent are tineas or dermatophytoses, tinea versicolor and tinea nigra and piedras (white and black). This chapter will refer to the latter four mycoses.1,2

Tinea versicolor
Tinea versicolor (pityriasis versicolor) is a superficial mycosis caused by various yeasts and lipophilic fungi of the genus Malassezia, with three dominant species: M globosa, M sympodialis, and M furfur. Tinea versicolor is characterized by the presence of fine scaly patches (pityriasis) or macules,
Corresponding author. E-mail address: a_bonifaz@yahoo.com.mx (A. Bonifaz). 0738-081X/$ see front matter 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.clindermatol.2009.12.004

which may be hypochromic or hyperchromic (versicolor), that are generally located on the upper aspects of the trunk, neck, and arms.3,4 It may extend to the face, groin, and even the thighs, whereas in children, the face is frequently involved. Tinea versicolor has been reported worldwide but is predominant in tropical climates. It has been found in newborns and elderly patients, although it is more frequent in young adults and is equally distributed between men and women. The most important predisposing factors are heat, humidity, use of oily tanning lotions and creams, and corticosteroids.3,5 The two clinical varieties are hypochromic or hypopigmented, which generally occurs in dark-skinned individuals and is characterized by hypochromic patches or macules covered with fine scales that are initially irregular with small borders that converge to form large patches (Figures 1 and 2). The hyperchromic or hyperpigmented variety consists of light brown patches with scales on the surface. Mixed cases may be found, especially in the axillary region, the groin, and the submammary folds. Both clinical varieties are asymptomatic, and only a few patients complain of itching.

Superficial mycoses

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Fig. 3

Retroauricular seborrheic dermatitis.

Although the hypochromic variety is observed in dark skin and the hyperchromic variety in fair skin, inverse cases may be found. It is important to distinguish both varieties from

Fig. 1

Hypochromic tinea versicolor.

Fig. 2

Hypochromic tinea versicolor (close-up).

Fig. 4 Folliculitis due to Malassezia is shown in panoramic and close-up views.

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A. Bonifaz et al. Seborrheic dermatitis is a benign, chronic, erythematosquamous dermatosis that has multiple causes. The most important factors are hormonal, environmental, psychologic, immunologic, and infectious (Malassezia spp). The most common manifestation is scalp scaling (dandruff). It can also affect the nasolabial folds, eyebrows, glabella, the retroauricular area, and the central region of the chest. Seborrheic dermatitis is generally asymptomatic, but some patients have mild pruritus (Figure 3). Malassezia spp are found in most cases, especially M globosa, M furfur, and M restricta. Seborrheic dermatitis is more frequent in patients with HIV infection. The use of topical and systemic antifungals decreases the signs and symptoms.2,4,7,8 Folliculitis due to Malassezia (FM) is a superficial infection of the pilosebaceous unit. M globosa, M furfur, and M pachydermatis are the species that have been isolated. FM usually affects the trunk, the shoulders, and exceptionally, the face. Clinically, it presents as pustules localized around the follicles without comedones, which distinguishes it from acne (Figure 4). Histologically, there is follicular dilatation and inflammatory infiltrate with yeast colonization. FM is more frequent in young adults and is considered an opportunistic infection.2,7 Onychomycosis due to the Malassezia spp is a rare infection that has caused controversy. Some cases associated with M globosa and M furfur have been reported. Clinically, it is a distal subunguial onychomycosis that is similar to dermatophytic infection. Some authors consider it

Fig. 5 Direct examination shows cluster yeast cells and short hyphae (potassium hydroxide and blue Parker stain; original magnification, 20).

pityriasis alba, hypochromic solar dermatitis, pityriasis rosea, and postlesional melanodermas.3,6 Rarely, tinea versicolor may occur in chronic cases as a papuloid variety; recently, atrophic and imbricata varieties have been reported.2,3,6 Among the infections caused by Malassezia spp (malassezioses) are a group of diseases related to these lipophilic yeasts. These microorganisms can be bystanders or the etiologic agent.2,7,8

Table 1 Superficial mycoses

Main characteristics of tinea versicolor, tinea nigra, white piedra, and black piedra Etiologic agent M. globosa M. sympodialis M. furfur Clinical location Upper part of the trunk, neck, arms Face (children) Clinical presentation Hypo-and hyperpigmented, macules with light scales Treatment Topical antifungals: imidazoles, terbinafine, ciclopiroxolamine Oral antifungals: ketoconazole, itraconazole, fluconazole Topical antifungals: imidazoles, ciclopiroxolamine Oral antifungals: ketoconazole, itraconazole

Tinea versicolor (Pityriasis versicolor)

Asymptomatic

Malassezioses Seborrheic dermatitis Folliculitis Onychomycosis Tinea nigra M. globosa M. sympodialis M. furfur M. restricta Hortae werneckii Scalp, central areas of face, eyebrows Trunk, shoulders Nails (hand) Palms and soles Erythematosquamous Folliculitis, pustules Distal subungual Brown to gray patches Asymptomatic

Control of hyperhidrosis

White piedra

T. cutaneum T. ovoides T. inkin Piedraia hortae

Black piedra

Scalp hairs Facial, axillary, and pubic hair Perianal hair (HIV patients) Asymptomatic Scalp hairs Black stone-like concretions Asymptomatic

Topical antifungals and keratolytics White stone-like concretions Shaving or clipping infected hairs Topical antifungals Keratolytics Shaving or clipping infected hairs Topical antifungals Keratolytics

Superficial mycoses a true infection, but others believe that the yeasts found are only carriers.2,4,7 Colonization by Malassezia has also been reported to be associated with diverse diseases such as atopic dermatitis, psoriasis, blepharoconjunctivitis, dacryocystitis, confluent and reticulated papillomatosis (Gougerot-Carteaud), systemic infections, and endocarditis.2,7 Laboratory diagnosis is made by skin scraping. Direct examination is done with 10% potassium hydroxide (KOH) solution, adding Parker blue ink (Quink Co.). Clusters of small blastoconidia or round budding yeast cells and short septate and, occasionally, branching filaments are observed (Figure 5). Cultures are not necessary for the diagnosis if a microscopic image is available. Cultures are performed on Sabouraud agar media plus antibiotics, adding 5% to 15% olive oil and Dixon's agar. They are incubated at 25 or 37C for 8 days and yield creamy, whitish-yellow colonies (Malassezia spp). Under the microscope, round or globus blastoconidia are generally observed, although they can be elongated, depending on the species. Woods light (ultraviolet) is very useful. Tinea versicolor patches or macules emit a characteristic yellow-green fluorescence. A biopsy specimen is not necessary. An inflammatory process may be observed. Filaments and yeast cells are found on the superficial layers of the skin and are easily visible with periodic acid-Schiff stain.2,4 Treatment consists of topical and systemic therapy. The first is recommended for limited or initial cases. Treatment must be administered for 2 to 4 weeks, as a minimum. Also useful are sodium hypochlorite (20%), propileneglycol (50%), and imidazoles, such as miconazole, clotrimazole, ketoconazole, bifonazole, as well as allylamines (terbinafine and naftifine) and ciclopiroxolamine. These antifungal drugs may be preferred in noncreamy forms, such as a gel and a spray, when available.3, 6 Systemic therapy is suggested in very extensive or recurrent cases. The three most recommended antifungals are ketoconazole, 200 mg/d for 7 to 15 days; itraconazole, 200 mg/d for 5 to 10 days; and fluconazole, 400 mg for 1 day.2,6,7 To avoid constant relapse, it is necessary to suppress predisposing factors as much as possible, especially excessive sun exposure, use of oily tanning lotions, and excessive sweating, which can be avoided by using desiccants (talcum powder; Table 1.

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Fig. 6

Tinea nigra presents as brown-black macules on the palm.

and frequently in children. The most important predisposing factor is hyperhidrosis of the hands and the feet. This is considered to be essential for development of fungal infection.9,11 The main clinical locations are the palms and sometimes the dorsal aspect of the hands, generally unilateral, and to a lesser degree, the soles, arms, legs, neck, and trunk. Tinea nigra is a chronic condition that presents as hyperpigmented, irregular, circumscribed patches or spots ranging in color from tan to dark brown or black, covered with fine scales, and usually asymptomatic (Figure 6).9-11 Laboratory diagnosis is performed by direct examination of the skin scales with 10% to 20% KOH solution. Dark, septate hyphae are observed with occasional clusters of yeast cells (blastoconidia; Figure 7). The usual cultures on Sabouraud agar media (28C) initially yield creamy colonies of yeast cells, which later become filamentous with hyphae and acropetal conidia. Biopsy specimens are not necessary

Tinea nigra
Tinea nigra is a superficial mycosis caused by a pigmented yeast, Hortaea werneckii (previously Phaeoannellomyces or Exophiala werneckii). It is a dematiaceous, polymorphic, halotolerant, and halophilic fungus; that is, it grows in an aqueous medium and adapts easily to hypersalinity.9,10 Most cases occur in tropical regions, especially coastal zones, and have been observed in young men and women

Fig. 7 Direct examination shows multiple dark, septate, hyphae, and yeast cells (10% potassium hydroxide stain; original magnification 10).

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A. Bonifaz et al.

Fig. 8 Dermoscopy of tinea nigra reveals a hyperpigmented fungal growth. (Photograph courtesy of Leonel Fierro, MD).

Fig. 10 Mycotic nodules (spores) of white piedra (10% potassium hydroxide stain; original magnification, 10).

for diagnosis. With hematoxylin and eosin stain, numerous pigmented spores and hyphae are observed at the level of the stratum corneum.7 Dermoscopy reveals a hyperchromic fungal growth stain. This technique is useful to differentiate tinea nigra from nevi, especially melanoma (Figure 8).12,13 Treatment is simple, because control of hyperhidrosis suffices. Keratolytics, such as 3% salicylic acid, Whitfield ointment, and topical antifungals such as bifonazole, clotrimazole, ketoconazole, terbinafine, and ciclopiroxolamine may be used. Oral itraconazole (100 mg/d) is effective (Table 1).9-11

White piedra
Piedra is the Spanish word for stone, and it was the original name of both white and black piedra. This is a superficial mycosis caused by yeast-like organisms of the genus Trichosporon, mainly T cutaneum, .n ovoide, and

T inkin. It is a chronic, asymptomatic infection that affects the hair shaft, preferably scalp hair shafts, and to a lesser extent, those of the beard, moustache, axillas and pubis, in the form of concretions or soft, whitish nodules.1,2,14 Most cases occur in tropical regions and are observed in young men and women and in children. The most important predisposing factors are humidity, hyperhidrosis, and poor personal hygiene.2 The most affected hairs are those of the scalp, but it may also be found in the axillae, pubis, and exceptionally, the beard, eyebrows, and eyelashes. White piedra is an asymptomatic condition. The hair is infected with small, soft concretions that are not initially visible and can only be palpated. A 1-to 3-mm whitish concretion with well-defined borders (Figure 9) subsequently develops, and a single shaft may have one to several concretions. It is important to differentiate the concretions from pediculosis (nits), trichorrhexis nodosa, monilethrix, and hair caps.2,15 Perianal hairs may have similar presentations in HIV-positive patients.16

Fig. 9

White piedra of scalp hairs.

Fig. 11 Mycotic nodules (spores) of black piedra. (10% potassium hydroxide stain; original magnification 40).

Superficial mycoses Laboratory diagnosis is performed with infected hairs treated with 10% to 20% KOH and examined under the microscope. They are made up of concretions formed by masses of septate hyphae with numerous septa and dense zones of arthroconidia (Figure 10). In cultures on Sabouraud agar media, etiologic agents yielded limited, similar, wet, yeast-forming colonies with a brain-shaped appearance. Identification is based on biochemical tests and micromorphologic aspects. Trichosporon species form true hyphae, arthroconidia, and blastoconidia.2,17 Treatment involves clipping the infected hairs; if the disease is widely disseminated, shaving the whole area is suggested. Subsequently, topical antifungals may be used, such as 1% mercury bichloride, 1% iodinated solution, or 30% salicylic acid solution. Good results have been reported with topical imidazoles such as econazole, isoconazole, or miconazole. The use of 2% ketoconazole shampoo is extremely effective and practical (Table 1).2,15

145 colonies and is identified by its micromorphology. The fungus presents a teleomorphic phase composed of fusiform asci and ascospores.1,18 Treatment for black piedra is the same as for white piedra: clipping infected hairs and applying a topical antifungal or keratolytic (Table 1).2

References
1. Schwartz RA. Superficial fungal infections. Lancet 2004;364:1173-82. 2. Bonifaz A. Micologa mdica bsica. 3rd ed. Mxico, DF: McGrawHill; 2009. p. 100-32. 3. Gupta AK, Batra R, Bluhm R, et al. Pityriasis versicolor. Dermatol Clin 2003;21:413-29. 4. Crespo-Erchiga V. Florencio VD. Malassezia yeasts and pityriasis versicolor. Curr Opin Infect Dis 2006;19:139-47. 5. Arenas R, Isa-Isa R, Cruz AC. Pitiriasis versicolor en Santo Domingo Repblica dominicana. Datos morfolgicos de Malassezia spp. In vivo en 100 casos. Rev Iberoam Micol 2001;18:29-32. 6. Padilla-Desgarenes MC. Pitiriasis versicolor. Dermatologa Rev Mex 2005;49:157-67. 7. Torres E, Arenas R, Atoche C. Infecciones causadas por el gnero Malassezia. Med Cut Lat Am 2008;36:265-84. 8. Ashbee HR. Update on the genus Malassezia. Med Mycol 2007;45: 287-303. 9. Bonifaz A, Badali H, de Hoog GS, et al. Tinea nigra by Hortaea werneckii, a report of 22 cases from Mexico. Stud Mycol 2008;61: 77-82. 10. Gupta AK, Chaudhry M, Elewski B. Tinea corporis, tinea cruris, tinea nigra, and piedra. Dermatol Clin 2003;21:395-400. 11. Perez C, Colella MT, Olaizola C, et al. Tinea nigra: report of twelve cases in Venezuela. Mycopathlogia 2005;160:235-8. 12. Hall J, Perry VE. Tinea nigra palmaris: differentiation from malignant melanoma or junctional nevi. Cutis 1998;62:45-6. 13. Xavier MH, Ribeiro LH, Duarte H, et al. Dermatoscopy in the diagnosis of tinea nigra. Dermatol Online J 2008;14:15. 14. Mndez-Tovar LJ, Rangel PT, Vega LF. Piedra blanca: caso clnico. Med Cut Lat Am 1996;24:26-8. 15. Kiken DA, Sekaran A, Antava RJ, et al. White piedra in children. J Am Acad Dermatol 2006;55:956-61. 16. Stenderup A, Schnheyder H, Ebbesen P, et al. White piedra and Trichosporon beigelii carriage in homosexual men. J Med Vet Mycol 1986;24:401-6. 17. Chagas-Neto TC, Chaves GM, Colombo AL. Update of the genus Trichosporon. Mycopathologia 2008;166:121-32. 18. Kanitakis J, Persat F, Piens MA, et al. Black piedra: report of a French case associated with Trichosporon asahii. Int J Dermatol 2006;45: 1258-60. 19. Figueras MJ, Guarro J, Zaror L. New findings in black piedra. Br J Dermatol 1996;135:157-8.

Black piedra
This is a superficial mycosis caused by Piedraia hortae, a pigmented fungus. It is a chronic, asymptomatic infection that generally affects the hair shafts of the scalp in the form of black, hard concretions or mycotic nodules.1,2 Most cases occur in tropical regions with high rainfall in young men and women and in children. The most important predisposing factors are humidity and poor personal hygiene.2,18 The disease is asymptomatic and is most frequently located on the hairs of the scalp, beard, and sporadically, the axillae and pubis. The morphology is very similar to that of white piedra. Brown or black, limited, spindle-shape hard concretions are formed with the appearance of grits or small stones, hence its name.18,19 Laboratory diagnosis is performed with infected hairs treated with 10% to 20% KOH and examined under the microscope. Pigmented brown ochre nodules are observed. Concretions are masses formed by pseudoparenchymal tissue that is made up of septate, thick-walled hyphae simulating arthroconidia. It is possible to see asci with two or more ascospores (this image is characteristic; Figure 11). In culture, the fungus grows at room temperature in Sabouraud agar media, presenting black-greenish, limited, acuminate