Pityriasis versicolor rubra

ARTICLE

Pityriasis versicolor (PV) is a chronic, benign and asymptomatic skin disease, which affects predominantly young adults of both sexes. It is composed of two color types, one of which is brown (pigmented), the other white (achromatic) [1]. Recently, a red colored type, PV rubra, has been reported by Horiuchi [2], Ohtani et al. [3] and Katoh et al. [4]. However, there was no identification of species of Malassezia. In this study, we report six similar cases of PV rubra, and identify the species M. sympodialis isolated from the scales of two different lesions at a 6 week-interval in the same person by the method of Makimura et al. [5]. Capillaroscopically, there was telangiectasis in the erythematous lesion, but neither in brown nor in white lesions. Therefore, we report the cases with discussion about the mechanism causing telangiectasis in the dermis.

Case reports

Case 1

A 46 year-old male with SLE, who has been treated by oral administration of corticosteroid (predonisolone; PSL15 mg/day) for four years and is well controlled, noticed erythema on the chest and trunk for one month in Oct, 1995. He noted neither fever nor general fatigue. Physical examination disclosed many soybean-sized or thumb-sized erythema (Fig. 1a), some of them with pigmentation. Differential diagnosis was seborrheic dermatitis, patch granuloma annulare [6] and annular erythema, etc, but neither induration nor pruritus was noticed. The scales on the erythema were clearly taken with Scotch-tape (Fig. 1b) and many sausage-like short segmented fungal elements were seen with positive Giemsa stain (Fig. 1c), although no confirmation was done by wood light. The results of laboratory investigations were within normal limits except for immunogloblin A (675 mg/dl), anti-nuclear (x 320, homogeneous & speckled types), anti-SS-A (x 59) and anti-SS-B (x 1.3) antibodies. Many small whitish colonies were grown on Sabouraud's agar culture containing cycloheximide (Mycosel) with olive oil. However, the strain was not identified. Capillaroscopically, the reddished lesions were confirmed as blood vessel dilatation (Fig. 1d, e). The lesion improved two weeks after application of anti-fungal ointment (isoconazole nitrate).

Case 2

A 57 year-old male with systemic scleroderma (SSc; diffuse type), who had been treated by oral administration of corticosteroid (PSL10 mg/day) and immuran (100 mg/day) for three years and was well controlled, noticed erythema on the back since Dec. 8, 1995. He noted neither pruritus nor pain. Physical examination disclosed several thumb-sized erythema. The scales on the erythema were clearly taken with Scotch-tape and many sausage-like short segmented fungal elements were seen with positive Giemsa stain, although no confirmation was done by wood light. The results of laboratory investigations were within normal limits except for immunogloblin A (148 mg/dl) and M (69 mg/dl), anti-nuclear (x 80, homogeneous and cytoplasmic types), anti-SS-A (x 8.6) antibodies. Many small whitish colonies were grown on Mycosel culture with olive oil. However, the strain was not identified. Capillaroscopically, the reddished lesions were confirmed as blood vessel dilatation. The lesion improved two weeks after application of anti-fungal ointment (isoconazole nitrate) without any pigmentation.

Case 3

A 21 year-old female with SLE, who had been treated by oral administration of corticosteroid (PSL15 mg/day) and mizoribin (150 mg/day) for eight years and was well controlled, noticed erythema on the chest and neck for one year in Nov., 1996. She applied anti-fungal ointment for the lesions, and the lesions recurred several times. However, she noted neither pruritus nor pain. Physical examination disclosed several soybean-sized or thumb-sized erythema. The scales on the erythema were clearly taken with Scotch-tape and many sausage-like short segmented fungal elements were seen with positive Giemsa stain, although no confirmation was done by wood light. The results of laboratory investigations were within normal limits except for anti-nuclear (x 320, homogeneous & speckled types), anti-SS-A (x 31.2) and anti-RNP (x 10.7) antibodies. Many small whitish colonies were grown on Mycosel with olive oil. However, the strain was not identified. Capillaroscopically, the reddished lesions were confirmed as blood vessel dilatation. The lesion improved two weeks after application of anti-fungal ointment (isoconazole nitrate).

Case 4

A 30 year-old female with SLE, who was treated by oral administration of corticosteroid (PSL15 mg/day) for two years and was well controlled, noticed several erythemous lesions on the right axillae for 1-2 years, and visited the Department of Dermatology of Prefectural Gifu Hospital on May 7, 1998. The results of laboratory investigations were within normal limits except for immunogloblin G (1,888 mg/dl) and complement (C₄; 15 mg/dl), anti-nuclear antibodies (x 160, homogeneous & speckled types). The scales on the erythema were clearly taken with Scotch-tape and many sausage-like short segmented fungal elements were seen with positive Giemsa stain, although no confirmation was done by wood light. The lesion improved two weeks after application of anti-fungal ointment (isoconazole nitrate) without any pigmentation.

Case 5

A 43 year-old female with Sjögren's syndrome who had been followed up in a clinic for five years and was well controlled, noticed erythema on the neck and the dorsum of the trunk every summer season for several years. She applied anti-fungal ointment on the lesions, but the lesions soon recurred. She noted slight surface hypersensitivity, but neither pruritus nor pain. Physical examination disclosed several soybean-sized or thumb-sized erythema on the neck and the dorsum of the trunk. The scales on the erythema were clearly taken with Scotch-tape and many sausage-like short segmented fungal elements were seen with positive Giemsa stain. The results of laboratory investigations were within normal limits except for anti-nuclear (x 320, homogeneous & speckled types), anti-SS-A (x 500) and anti-SS-B (x 110) antibodies. Many small whitish colonies were grown on Mycosel culture with olive oil. However, the strain was not identified. The lesion improved two weeks after application of anti-fungal ointment (isoconazole nitrate). Histopathological features of the lesion on the dorsum of the trunk showed no epidermal hyperplasia without elongation of rete ridges and no inflammatory cell infiltration in the dermis, which revealed neither seborrheic dermatitis nor patch granuloma annular as reported by Mutasim and Bridges [6], however, there was only dilatation of small blood vessels in the dermis. In the horny layers, many yeastlike or fine filamentous structures with PAS and Grocott stains were seen (not shown).

Case 6

A 31 year-old male noticed erythema on the dorsum of the trunk and the chest for 1 month, and visited the Department of Dermatology of Prefectural Gifu Hospital on June 3, 1999. He was in good general health. Physical examination disclosed many thumb-sized erythema on the dorsum of the trunk (Fig. 2a) and soybean-sized erythema on the chest (Fig. 2b). The scales on the erythema were clearly taken with Scotch-tape and many sausage-like short segmented fungal elements were seen with positive Giemsa stain (Fig. 2c) as well as previous cases. The results of routine laboratory investigations were within normal limits. Several whitish colonies were grown on Mycosel culture with olive oil from both lesions of the chest and the dorsum of the trunk.

Histopathological features of the lesion on the dorsum of the trunk showed no epidermal hyperplasia without elongation of rete ridges and only dilatation of small blood vessels without any inflammatory cell infiltration in the dermis (Fig. 2d). Telangiectasis was reconfirmed capillaroscopically as well as in Case 1. In the horny layers, many yeastlike or fine filamentous structures with PAS and Grocott stains were seen (Fig. 2e). Both clinical and histopathological features led to speculation of PV infection. M. sympodialis was identified from the lesion of the chest, and again from the lesion of the dorsum of the trunk. The patient was treated with antifungal ointment (bifonazole), and the lesions on the chest diminished within two weeks.

All above cases were found from May, 1995 through June, 1999, however, no reccurrence has been seen in these years.

Patch test using the strains of PV rubra and nigra

In two healthy controls (a 51 year-old male and a 25 year-old female), patch tests using cultured Malassezia strain obtained from the erythematous and pigmentous lesion in a case of a 33 year-old male with PV rubra (left side of neck) and nigra (right axillae) were carried out for 48 hours. As a result, there were slightly capillaroscopical telangiectatic changes in the patch test lesion using the strain obtained from the erythematous lesion of PV rubra, but no change in the brown lesion of PV nigra in the male (not shown), although there was a negative reaction in both patch tests in both healthy controls.

Discussion

Malassezia yeasts isolated from human skin were classified in two morphological and clinical entitiles, Pityrosporum ovale associated with pityriasis capitis and seborrheic dermatitis and Pityrosporum orbiculare with PV and other human cutaneous diseases [7]. As a result of taxonomic analysis of the genus Malassezia by using morphology and molecular biology such as DNA/DNA complementary and LSU rRNA sequence similarity [8], the genus has been enlarged to include seven species [9]; one lipid-independent species, M. pachydermatis and six lipid-dependent species, M. furfur, M. sympodialis, M. globosa, M. obtusa, M. restricta and M. slooffiae.

In this study, we have neither experienced the transformation of PV rubra to nigra nor alba as indicated by Horiuchi [2]. He reported four cases of PV rubra; two of them transformed PV rubra into nigra (25 and 39 year-old males) and one into alba (36 year-old male) three days after the application of anti-fungal ointment (isoconazole). He reported no background of systemic autoimmune diseases such as SLE, SSc and Sjögren's syndrome. Although the combination of both PV rubra and nigra was seen in our three cases (No. 1, 2 and 3 in Table I), these clinical data may reveal that PV rubra has no relation to PV nigra. Subsequently, it is possible that PV rubra is independent from PV nigra, but it is not sure. Systemic autoimmune diseases such as SLE, SSc and Sjögren's syndrome were present in five of our cases, but some immunological disorder may not be closely related to the occurrence of PV rubra as well as PV nigra and alba. Although Ohtani et al. [3] reported three middle aged males (45, 46 and 53 year-old) with PV rubra without any description of their clinical course and background in a meeting (only abstract is available), Katoh et al. [4] found that an erythematous lesion in a 46 year-old male with PV rubra cured with pigmentation two weeks after the application of anti-fungal ointment (ranoconazole). A review of the literature showed only 8 cases including Ohtani et al. [3] and Katoh et al. [4], however, the causative fungus in all cases was not detected.

This article reports an interesting case caused by M. sympodialis, which was reconfirmed twice, because Makimura et al. [5] reported that 7 strains were isolated from PV, 3 from seborrhoeic dermatitis, 1 from atopic dermatitis and 11 from healthy controls; in all 22 strains of M. sympodialis. M. sympodialis is the predominant species in the healthy trunk, because Erchiga et al. [1] reported that M. sympodialis was also found in 16 of 43 healthy skin samples from PV. Additionally, M. sympodialis is also isolated from dogs [10] and cats [11, 12] as well as human normal skin [13, 14]. However, M. sympodialis triggers the severe form of common cephalic pustulosis (neonatal acne) in infants with this benign disorder [15] and malignant otitis externa [16], which is a very rare systemic infection.

It is still unclear whether this strain is closely associated to the pathogenesis for occurrence of PV rubra or not. However, the strain may stimulate blood vessel dilatation in the dermis, because patch test using cultured strain from the lesions of PV rubra and nigra in one of two healthy controls revealed telangiectasis capillaroscopically in the former patch tested lesion. Therefore, the strain from PV rubra may be related to the function of blood vessel dilatation in the dermis. Further detailed investigation of the functional cause of telangiectasis, including several cytokines, will be needed in the future.

Article accepted on 1/10/01

REFERENCES

1. Erchiga VC, Martos AO, Casaño AV, Erchiga AC, Fajardo FS, Guého E. Mycology of pityriasis versicolor. J Mycol Med 1999; 9: 143-8.

2. Horiuchi Y. Pityriasis versicolor rubra. Hifubyo-shinryo 1989; 11: 578-80 (in Japanese).

3. Ohtani M, Oyamada T, Kondo M, Miwa T. Tinea versicolor rubra (TVR). J JOCD 1994; 42: 207 (in Japanese).

4. Katoh T, Hisamatsu Y. Pityriasis versicolor. Hifubyo-shinryo 1997; 19: 613-4 (in Japanese).

5. Makimura K, Tamura Y, Kudo M, Uchida K, Saito H, Yamaguchi H. Species identification and strain typing of Malassezia species stock strains and clinical isolates based on the DNA sequences of nuclear ribosomal internal transcribed spacer 1 regions. J Med Microbiol 2000; 49: 29-35.

6. Mutasim DF, Bridges AG. Patch granuloma annulare: clinicopathologic study of 6 patients. J Am Acad Dermatol 2000; 42: 417-21.

7. Guillot J, Guého E, Lesourd M, Midgley G, Chévrier G, Dupont B. Identification of Malassezia species, a practical approach. J Mycol Med 1996; 6: 103-10.

8. Guillot J, Guého E. The diversity of Malassezia yeasts confirmed by rRNA sequence and nuclear DNA comparisons. Antonie Van Leeuwenhoek 1995; 67: 297-314.

9. Guého E, Midgley G, Guillot J. The genus Malassezia with description of four new species. Antonie Van Leeuwenhoek 1996; 69: 337-55.

10. Raabe P, Mayser P, Weiss R. Demonstration of Malassezia furfur and M. sympodialis together with M. pachydermatis in veterinary specimens. Mycoses 1998; 4: 493-500.

11. Crespo MJ, Abarca ML, Cabanes FJ. Otitis externa associated with Malassezia sympodialis in two cats. J Clin Microbiol 2000; 38: 1263-6.

12. Bond R, Howell SA, Haywood PJ, Lloyd DH. Isolation of Malassezia sympodialis and Malassezia globosa from healthy pet cats. Vet Rec 1997; 141: 200-1.

13. Aspiroz C, Moreno LA, Rezusta A, Rubio C. Differentiation of three biotypes of Malassezia species on human normal skin. Correspondence with M. globosa, M. sympodialis and M. restricta. Mycopathologia 1999; 145: 69-74.

14. Bond R, Anthony RM, Dodd M, Lloyd DH. Isolation of Malassezia sympodialis from feline skin. J Med Vet Mycol 1996; 34: 145-7.

15. Niamba P, Weill FX, Sarlangue J, Labreze C, Couprie B, Taieh A. Is common neonatal cephalic pustulosis (neonatal acne) triggered by Malassezia sympodialis? Arch Dermatol 1998; 134: 995-8.

16. Chai FC, Auret K, Christiansen K, Yuen PW, Gardam D. Malignant otitis externa caused by Malassezia sympodialis. Head Neck 2000; 22: 87-9.