Review

Tinea versicolor in dark-skinned individuals Joseph R. Kallini1, MD, Fauzia Riaz2, MD, and Amor Khachemoune3, MD, FAAD, FACMS

1 Eisenhower Medical Center, Rancho Mirage, CA and Baylor College of Medicine, Houston, TX, 2Department of Internal Medicine, Georgetown University Medical Center, Washington, DC, and 3Veterans Affairs Medical Center, Brooklyn, NY, USA

Abstract In this article, we review the salient features of tinea versicolor and describe the epidemiology, clinical presentation, and histopathology of this mycosis in dark-skinned individuals. Tinea versicolor is caused by an overgrowth of the Malassezia genus. It manifests clinically as asymptomatic hypopigmented macules, hyperpigmented macules, or a combination of the two. Under light microscopy, Malassezia presents as a dimorphic

Correspondence Amor Khachemoune, MD, FAAD, FACMS Veterans Affairs Medical Center 800 Poly Place Brooklyn, NY 11209, USA E-mail: [email protected]

fungus – in both the hyphal and yeast form. Most clinicians have found that the majority of dark-skinned patients present solely with hypopigmented lesions. Under light microscopy, lesions on dark skin involved with tinea versicolor tend to have a thicker stratum corneum, more tonofilaments in the granulosum, and more sequestered melanosomes. Differential diagnosis includes confluent and reticulated papillomatosis, seborrheic dermatitis, pityriasis rosea, pityriasis alba, and vitiligo. Tinea versicolor can be successfully managed in most

Conflicts of interest: None.

cases with topical antifungal treatments. Cases of recurrence, such as those seen in immunocompromised patients, may necessitate scheduled oral or topical therapy.

Introduction Tinea versicolor is a cutaneous condition caused by an overgrowth of the Malassezia genus, which is a fungal component of the normal skin flora commonly found in the seborrheic regions of the face, arms, and trunk.1–3 It presents clinically with either hypopigmented or hyperpigmented macules or a combination of the two.3 As with many skin conditions, it is imperative to take note of the differences in the way tinea versicolor presents in darkskinned versus light-skinned individuals. In this article, we summarize the salient features of tinea versicolor with a focus on dark-skinned patients. Etiology Tinea versicolor is a cutaneous mycosis caused by fungi of the Malassezia genus. Currently, the most common causative species is Malassezia globosa.4 M. furfur is the next most common species, with other causes being M. sympodialis, M. sloffiae, and M. restricta.3,5 At present, there is no determined difference between the causative species of tinea versicolor in dark-skinned patients versus that of light-skinned patients documented in the literature. Malassezia is a small fungus composed of only 9 Mb of genetic material. Because of this, its inhabitance is limited to normal skin flora of humans and other vertebrates. This fungus is not very resilient; all are unable to grow in non-lipid-containing media (with the exception of M. pachydermatis).6 Despite the similar habitat, Malaª 2013 The International Society of Dermatology

ssezia is not phylogenetically related to other common epidermal fungi, such as the dermatophytes and Batrachochytrium genus. The reproductive cycle of Malassezia is unclear: a region corresponding to a mating type locus (MAT) and genes governing meiosis have been identified for M. globosa – suggesting that the mating pattern is sexual rather than asexual.6 Immunocompetent hosts usually eliminate virulent Malassezia via monocyte-derived dendritic cells that bind and phagocytize the organisms; these are activated via the adaptive T-helper cell immune response.6 There are several contributing factors that can increase the likelihood of pathologic overgrowth of this fungus.3 These include application of oily preparations and creams (due to the lipophilicity of the organisms), an increase in environmental humidity, corticosteroid overuse, and genetic predilection. Furthermore, as with other pathogens, disruption of the epidermal barrier (common in individuals with atopic eczema) may precipitate sensitization and allergen-specific IgE and T-cell reactivity to the fungus. In addition, the lack of antimicrobial peptides such as LL-37 and human beta-defensin-2 (HBD-2) may precipitate pathology.6 Indeed, tinea versicolor is prevalent in tropical environments. In tinea versicolor, the species present in the dimorphic form – as a combination of short, septate, non-branched pseudohyphae along with the round spore form.3 The pathophysiology of hypopigmented lesions differs from that of hyperpigmentation. It was hypothesized that hypopigmented macules have been caused by damage to International Journal of Dermatology 2014, 53, 137–141

137

138

Review

Tinea versicolor

melanocytes, inhibition of tyrosinase by dicarboxylic acid produced by Malassezia, and by the accumulation of lipid-like material in the stratum corneum blocking ultraviolet light.1,7 Hyperpigmented macules may be due to inflammation directly caused by Malassezia.8 One study comparing punch biopsy specimens from four patients with tinea versicolor demonstrated that there might be differences in the pathophysiology of tinea versicolor in dark-skinned versus light-skinned patients. Under light microscopy, dark skin involved with tinea versicolor tends to have a thicker stratum corneum than hypopigmented skin. Furthermore, the granular layer of involved dark skin has more tonofilaments. Melanosomes are usually transferred from melanocyte to keratinocyte via the release of multiple globules of melanin into the extracellular space from melanocytes followed by subsequent ingestion by keratinocytes. In dark-skinned individuals, the melanosomes are more numerous and originate from many melanocytic dendrites. They are also more densely packed with pigmented globules than lightskinned individuals.9 Owing to the high melanocytic density deposited into the extracellular space by melanocytes, it is possible that keratinocytes in dark-skinned patients tend to have more difficulty ingesting melanosomes.10 Epidemiology in dark-skinned individuals Several studies have found that the incidence of tinea versicolor remains uniform across different climates and ethnicities.11,12 Berry and Khachemoune12 found that there is no evidence that this condition is more prevalent in darker versus lighter skin, though the presentation may be more visually apparent in dark-skinned individuals. On the other hand, Child et al.13 found a statistically significant predilection for tinea versicolor for darker skin types in southeastern London; 48% in black people compared to 35% in white. Furthermore, Faye et al.14 state that the most common cause of hypopigmented patches in the rural West African state of Mali was tinea versicolor. It has also been shown that there is more facial and neck involvement in black people as opposed to the torso.15–17 There is evidence indicating higher prevalence of tinea versicolor in males, regardless of ethnicity, due to increased sebaceous activity.2,11 Additionally, there is a higher predilection for adolescents, indicating a possible relation to hormones and androgens.11 Clinical presentation in dark-skinned individuals Tinea versicolor presents initially as a hyperpigmented or hypopigmented 3–5 mm round or oval macule. Over International Journal of Dermatology 2014, 53, 137–141

Kallini et al.

time, multiple macules form and coalesce, leading to irregularly-shaped patches affecting a greater portion of the body.3,12 The skin dyspigmentation is most often the presenting complaint.1 The lesions are asymptomatic and have a predilection for the trunk and proximal aspects of the upper and lower extremities. Gentle scraping of the lesion produces a fine superficial scale.18 Several studies have indicated that most darker-skinned patients present with hypopigmentation rather than hyperpigmentation.3,12,18–20 The reason for this is unclear; the authors have seen no correlation with hygiene, socioeconomic status, or associated dermatoses. Studies in dark-skinned Indian populations have concluded that 75–85% of their patients present with hypopigmentation, 5–15% with mixed lesions, and the small remainder with hyperpigmentation.2,19,21 A notable exception is the study by Aljabre et al.1 of 100 darkskinned patients in King Fahd Hospital in Saudi Arabia; as high as one-third of dark-skinned patients presented with hyperpigmented lesions. A possible confounder to this result may have been the variance in climate of the different study populations.19 Nevertheless, cases of hyperpigmented lesions on dark-skinned patients do exist. One case report describes a 35-year-old African-American man with dark lesions on his abdomen.22 Another case describes a 16-year-old African-American girl with hyperpigmented tinea versicolor on her eyelids.23 Lastly, two African-American men have presented to our clinic in New York, both with hyperpigmented, scaly macules coalescing into patches on the abdomen and back (Figs. 1–3). Moreover, hyperpigmented lesions of tinea versicolor in dark-skinned patients may appear clinically distinct from hyperpigmented lesions in light-skinned patients. Hyperpigmented tinea versicolor may present as dark brown to gray–black macules and patches in those with dark skin, while hyperpigmented lesions are often light brown in lighter skin.7 Although unclear in present literature, we hypothesize that the variation in appearance of these lesions may be due to the differences in ultrastructural composition already present in healthy dark versus light skin (see Etiology). Tinea versicolor may present in many unusual ways in dark-skinned patients. One case report describes a 65-year-old man with a presentation mimicking pityriasis rubra pilaris: multiple orange–red, scaly plaques throughout the body with unusually extensive islands of sparing over the chest and back. His palms and soles were thickened, and fissures were noted over the hands.12 Another phenomenon uniquely attributed to AfricanAmericans is colloquially known as acid skin. This is the formation of coalescent hypopigmented plaques because of recurrent tinea versicolor and other papulosquamous disorders. The name had arisen because of a belief among ª 2013 The International Society of Dermatology

Kallini et al.

Figure 1 On the abdomen of this African-American man, tinea versicolor presents as hyperpigmented macules coalescing into patches. Fine scaling can also be appreciated

Tinea versicolor

Review

Figure 3 Another African-American man presents with hyperpigmented tinea versicolor

One sequela of tinea versicolor is postinflammatory hyperpigmentation (PIH), which occurs more often in dark-skinned individuals.26 Differential diagnosis Many dermatoses have been determined to be more common in dark-skinned individuals: acne vulgaris (the most common), eczema, disorders of pigmentation, seborrheic dermatitis, and alopecia.15 Several other conditions have been associated with Malassezia. To differentiate these cases from tinea versicolor, a skin biopsy is the gold standard.18 An important differentiating characteristic is that other conditions caused by Malassezia appear only in the yeast form, whereas the fungus in tinea versicolor appears in the dimorphic form.3 This is referred to as spaghetti and meatballs under potassium hydroxide preparation, where spaghetti represents the pseudohyphae and meatballs the round spores. The differential diagnoses of tinea versicolor in darkskinned individuals are listed in Table 1. Figure 2 On the back of this African-American man, tinea versicolor presents as hyperpigmented macules coalescing into patches

African-Americans that this condition is due to ingestion of acidic foods – such as carbonated beverages and protein-rich foods. However, this is false.24 Treatment of the underlying condition usually resolves the lesions.25 ª 2013 The International Society of Dermatology

Management At present, the treatment guidelines for tinea versicolor in dark-skinned individuals are identical to those with lighter skin. We propose that cutaneous lesions in darkskinned patients be treated more aggressively due to the increased incidence of postinflammatory pigmentary changes that occur in these patients. In most cases, tinea International Journal of Dermatology 2014, 53, 137–141

139

140

Review

Tinea versicolor

Kallini et al.

Table 1 Differential diagnosis of tinea versicolor Seborrheic dermatitis Pityriasis rosea Vitiligo Erythrasma Pityriasis alba Secondary syphilis Confluent and reticulated papillomatosis of Gougerot and Carteaud Mycosis fungoides

Presents with a more erythematous plaque and typically has a thicker scale. Predilection for the trunk but can be commonly found on the scalp, eyebrows, and nasolabial folds Presents with more erythematous and inflammatory macules in a “Christmas-tree like” distribution on the trunk. Additionally, in dark-skinned people the lesions are commonly hyperpigmented Presents with completely depigmented macules and patches Present with either erythematous or hyperpigmented patches with a predilection for the axilla and groin Presents with hypopigmented macules and patches on the face and upper extremities. Commonly found in children Presents with erythematous to brown macules or plaques. Found in a generalized distribution with involvement of palms and soles Presents with hyperpigmented, reticulated, scaly patches. Commonly found in young adults

Presents with hypopigmented patches and, to a lesser degree, erythematous plaques with fine scale. Commonly found on the trunk and extremities

versicolor can be successfully managed with topical antifungal treatments. Commonly prescribed medications include 2.5% selenium and 2% ketoconazole, both of which have antimicrobial activity. In more severe cases, oral antifungals have been shown to be effective, including ketoconazole, itraconazole, and fluconazole.12,20 There has also been a published report showing some success in treating with 5-aminolevulinic acid photodynamic therapy, though there have not been any published clinical trials.27 Patients who have repetitive infections of tinea versicolor, such as those who are immunocompromised, can prevent recurrences with regimented oral or topical therapy. Oral itraconazole and ketoconazole can be used for prophylactic treatment of tinea versicolor.28,29 Despite these various therapies, there is a high recurrence rate of tinea versicolor – with no differentiation between initial use of topical versus oral antifungals. Systemic therapy is indicated in situations where there have been recurrent infections. Prophylactic use of an oral imidazole once a month can prevent recurrent infections.29,30 Though both oral fluconazole and itraconazole are used for prophylaxis, there is some evidence from adult studies indicating that relapses are less frequent with fluconazole.31 Topical selenium sulfide 2.5% or ketoconazole 2% shampoo applied to the entire body for 10 minutes once a month is also effective. Resistance to therapy, frequent recurrence, or widespread disease should prompt consideration of an immunodeficient state.31 It is also important to note that postinflammatory dyspigmentation associated with tinea versicolor, as seen more often in those with darker skin, can persist for several months despite adequate and successful treatment of the infection. In these cases, a potassium hydroxide preparation can be useful to distinguish lingering skin changes from enduring or continued disease. The primary treatment of PIH secondary to tinea versicolor is prevention. This includes photoprotection International Journal of Dermatology 2014, 53, 137–141

– avoiding sunlight, wearing protective clothing, using lotions with sun protective factor (SPF) 15 or greater, and avoiding photosensitive medications. Patients are also encouraged to avoid unnecessary trauma – picking, rubbing, and scratching. Aside from prevention, a number of medications are used in the treatment of PIH. Hydroquinone is the gold standard; its mechanism of action is inhibition of tyrosinase, which converts dihydroxyphenylalanine (DOPA) to melanin, thus inhibiting repigmentation. This is best used with sunscreen as ultraviolet radiation hinders the effects of hydroquinone. Concomitant use of ascorbic acid, alphahydroxy acids, and other oxidants also increased the efficacy. Topical retinoids (tretinoin 0.01–0.1%, adapalene 0.1%, and tazarotene 0.1%) are also used for PIH. Their mechanism of action is to inhibit the transcription of tyrosinase. Other medications that inhibit tyrosinase include arbutin, kojic acid, licorice extract, and N-acetyl glucosamine (which specifically inhibits glycosylation). Niacinamide is a medication that acts by inhibiting the transfer of melanosomes.26 Conclusion Tinea versicolor is a cutaneous mycosis caused by the Malassezia genus, most commonly M. furfur. Tinea versicolor presents as hyperpigmented or hypopigmented round or oval macules that grow numerous and coalescent over time. Although the etiology is unchanged, this condition has been found to have varying clinical presentation based on skin color. There are conflicting findings in regards to the prevalence of tinea versicolor in different skin colors; some show no correlation while others find a predilection for darker individuals. In dark-skinned individuals, most studies have shown that hypopigmentation is more common. PIH is also more common in darkskinned patients. Under microscopy, the lesions of darkskinned patients have a thicker stratum corneum, more ª 2013 The International Society of Dermatology

Kallini et al.

tonofilaments, and more sequestered melanosomes. The differential diagnosis of tinea versicolor includes pityriasis rosea, pityriasis alba, seborrheic dermatitis, vitiligo, and others. It is treated similarly in all skin colors: with topical antifungals in less severe cases and oral antifungals in more severe cases. Despite these treatments, there is a high recurrence rate of tinea versicolor. Monthly preventative therapy with these medications may be used for patients with recurrence. References 1 Aljabre SH, Alzayir AA, Abdulghani M, et al. Pigmentary changes of tinea versicolor in dark-skinned patients. Int J Dermatol 2001; 40: 273–275. 2 Rao GS, Kuruvilla M, Kumar P, et al. Clinicoepidemiological studies on tinea versicolor. Indian J Dermatol Venereol Leprol 2002; 68: 208–209. 3 Tovar LM. Pathogenesis of dermatophytosis and tinea versicolor. Clin Dermatol 2010; 28: 185–189. 4 Morishita N, Sei Y. Microreview of pityriasis versicolor and Malassezia species. Mycopathologia 2006; 162: 373–376. 5 Krisanty RI, Bramono K. Made Wisnu I. Identification of Malassezia species from pityriasis versicolor in Indonesia and its relationship with clinical characteristics. Mycoses 2009; 52: 257–262. 6 Saunders CW, Scheynius A, Heitman J. Malassezia fungi are specialized to live on skin and associated with dandruff, eczema, and other skin diseases. PLoS Pathog 2012; 8: e1002701. 7 Nazzaro-Porro M, Passi S. Identification of tyrosinase inhibitors in cultures of Pityrosporum. J Invest Dermatol 1978; 71: 205. 8 Galadari I, el Komy M, Mousa A, et al. Tinea versicolor: histologic and ultrastructural investigation of pigmentary changes. Int J Dermatol 1992; 31: 253. 9 Ando H, Niki Y, Ito M, et al. Melanosomes are transferred from melanocytes to keratinocytes through the processes of packaging, release, uptake, and dispersion. J Invest Dermatol 2012; 132: 1222–1229. 10 Karaoui R, Bou-Resli M, Al-Zaid NS, et al. Tinea versicolor: ultrastructural studies on hypopigmented and hyperpigmented skin. Dermatologica 1981; 162: 69–85. 11 Belec L, Testa J, Bouree P. Pityriasis versicolor in the Central African Republic: a randomized study of 144 cases. J Med Vet Mycol 1991; 29: 323–329. 12 Berry M, Khachemoune A. Extensive tinea versicolor mimicking Pityriasis rubra pilaris. J Drugs Dermatol 2009; 8: 490–491. 13 Child FJ, Fuller LC, Higgins EM, et al. A study of the spectrum of skin disease occurring in a black population in south-east London. Br J Dermatol 1999; 141: 512–517.

ª 2013 The International Society of Dermatology

Tinea versicolor

Review

14 Faye O, NDiaye HT, Keita S, et al. High prevalence of non-leprotic hypochromic patches among children in a rural area of Mali, West Africa. Lepr Rev 2005; 76: 144–146. 15 Halder RM, Nandedkar MA, Neal KW. Pigmentary disorders in ethnic skin. Dermatol Clin 2003; 21: 617–628, vii. Review. 16 Pontasch MJ, Kyanko ME, Brodell RT. Tinea versicolor of the face in black children in a temperate region. Cutis 1989; 43: 81–84. 17 Testa J, Belec L, Bouree P. Epidemiological survey of 126 cases of pityriasis versicolor in the Central African Republic. Ann Soc Belg Med Trop 1991; 71: 153–154. 18 MacKie R. Clinical Dermatology, 4th edn. New York: Oxford University Press, 1997. 19 Ghosh SK, Dey SK, Saha I, et al. Pityriasis versicolor: a clinicomycological and epidemiological study from a tertiary care hospital. Indian J Dermatol 2008; 53: 182–185. 20 Gupta AK, Batra R, Bluhm R, et al. Skin diseases associated with Malassezia species. J Am Acad Dermatol 2004; 51: 785–798. 21 Krishnan A, Thapa DM. Morphological and pigmentary variations of tinea versicolor in south Indian patients. Indian J Dermatol 2003; 48: 83–86. 22 Usatine RP. Variations in color. J Fam Pract 2003; 52: 481–484. 23 Huang WW, Tharp MD. A case of tinea versicolor of the eyelids. Pediatr Dermatol 2012. doi: 10.1111/j.15251470.2012.01753.x [Epub ahead of print]. 24 Hall JC. Sauer’s Manual of Skin Diseases, 9th edn. Philadelphia, PA: Lippincott Williams & Wilkins, 2006. 25 VanDersarl JV, Arnold WL. Acid skin in black patients. Arch Dermatol 1983; 119: 627. 26 Callender VD, St Surin-Lord S, Davis EC, et al. Postinflammatory hyperpigmentation: etiologic and therapeutic considerations. Am J Clin Dermatol 2011; 12: 87–99. 27 Kim YJ, Kim YC. Successful treatment of pityriasis versicolor with 5-aminolevulinic acid photodynamic therapy. Arch Dermatol 2007; 143: 1218–1220. 28 Faergemann J, Gupta AK, Al Mofadi A, et al. Efficacy of itraconazole in the prophylactic treatment of pityriasis (tinea) versicolor. Arch Dermatol 2002; 138: 69–73. 29 Rausch LJ, Jacobs PH. Tinea versicolor: treatment and prophylaxis with monthly administration of ketoconazole. Cutis 1984; 34: 470–471. 30 Rai MK, Wankhade S. Tinea versicolor – an epidemiology. J Microbial Biochem Technol 2009; 1: 051–056. 31 Pantazidou A, Tebruegge M. Recurrent tinea versicolor: treatment with itraconazole or fluconazole? Arch Dis Child 2007; 92: 1040–1042. Review.

International Journal of Dermatology 2014, 53, 137–141

141

Tinea versicolor in dark-skinned individuals.

In this article, we review the salient features of tinea versicolor and describe the epidemiology, clinical presentation, and histopathology of this m...
154KB Sizes 0 Downloads 0 Views