article information

Jundishapur Journal of Microbiology: Vol.6, issue 6; e8581
published online: August 1, 2013
article type: Research Article
received: October 20, 2012
revised: January 11, 2013
accepted: February 23, 2013
DOI: https://doi.org/10.5812/jjm.8581
Crossmark

Identification of Malassezia Species Isolated From Patients With Pityriasis Versicolor in Sari, Iran, 2012

authors:

avatar Parvaneh Afshar 1 , avatar Maryam Ghasemi ORCID 2 , * , avatar Shamsi Kalhori 3

Referral Laboratory, Mazandaran University of Medical Sciences, Sari, IR Iran
Department of Pathology, School of Medicine, Mazandaran University of Medical Sciences, Sari, IR Iran
Mazandaran University of Medical Sciences, Sari, IR Iran

how to cite: Afshar P, Ghasemi M, Kalhori S. Identification of Malassezia Species Isolated From Patients With Pityriasis Versicolor in Sari, Iran, 2012. Jundishapur J Microbiol. 2013;6(6):e8581. https://doi.org/10.5812/jjm.8581.

Abstract

Background:

The genus Malassezia is part of the normal mycota of the skin of humans and other warm-blooded animals as etiological agents of pityriasis versicolor.

Objectives:

Several species from the Malassezia genus are known based on morphological, biochemical and molecular approaches. Therefore, the aim of this study was to determine the distribution of Malassezia species in patients with pityriasis versicolor based on morphological, physiological and biochemical criteria in Sari, Iran.

Materials and Methods:

In total, among 134 patients clinically suspected of having pityriasis versicolor, attending the Department of Mycology, Boali Sina Hospital and Referral Laboratory of the Mazandaran University of Medical Sciences, 116/134 (86.5%) positive patients for Malassezia elements, namely, yeast cells and short hyphae in microscopic examination, were included in the study. All 116 samples were inoculated on plates containing modified Leeming and Notman agar medium and identified at species level based on mycological criteria.

Results:

However, only 100/116 (86.2%) or 100/134 (74.6 %) of the patients showed Malassezia spp in culture. Malassezia. globosa (54%) was the most commonly isolated species followed by M. furfur (32%), M. slooffiae (6%), M. restricta (6%) and M. sympodialis (2%). Mixed Malassezia species were not identified.

Conclusions:

M. globosa was found to be the predominant pityriasis versicolor isolate in Sari, Iran. Since Malassezia species show different responses in their antifungal therapy, thus correct identification of Malassezia species and antifungal susceptibility test could facilitate selection of appropriate antifungal agents.

1. Background

Malassezia yeasts are lipophilic fungi which are regarded as normal flora of the skin, and are recovered in 75–98% of healthy individuals (1-3). Malassezia yeasts may also have a role in pityriasis versicolor (4), seborrhoeic dermatitis (5, 6), dandruff (6), seborrhoeic blepharitis (7), Malassezia folliculitis (8), confluent, reticulate papillomatosis (9) and uncommon systemic infections. In the last category, Malassezia species are associated with catheter acquired sepsis, fungaemia and pulmonary infection in neonates; these infections can sometimes be life threatening (10-14) and have been reported as significant causes of fungal infections in patients with cancer (15, 16) and HIV positive individual (17).

The difficulty in culturing Malassezia spp. in vitro has delayed the determination the taxonomic status of these yeasts. Nowadays, morphological characteristics and physiological features, the use of different Tween compounds as well as molecular studies of Malassezia species have allowed their classification into 11 species; M. furfur, M. sympodialis, M. slloffiae, M. obtusa, M. globosa, M. restricta, M. pachydermatis, M. yamatoensis, M. nana, M. japonica and M. dermatis (18, 19). Since molecular methods are not cost effective and unavailable in clinical laboratories, thus the purpose of this study was to identify Malassezia species isolated from pityriasis versicolor patients in Sari, Iran, by conventional methods, based on morphological, physiological and biochemical techniques (20).

2. Materials and Methods

2.1. Sample Collection

This cross sectional study was conducted between Octobers 2011 to April 2012 and a total of 134 patients clinically suspected of pityriasis versicolor, attending the Department of Mycology, Boali Sina Hospital and Referral Laboratory of the Mazandaran University of Medical Sciences were consecutively included. Individuals who received local or systemic antifungal for at least 5 days or corticosteroid agents for 3 weeks before the mycological examination were excluded from the study.

Skin scrapings were taken from the scaliest sites and obtained by the use of sterile blades. The diagnosis of pityriasis versicolor was established by the presence of both hyphae and spores in direct microscopy with KoH 20% and methylene blue staining. The assessed samples were plated onto Sabouraud's dextrose agar (SDA, Difco)(1% w/v peptone, 1% w/v glucose, 0.2% w/v yeast extract, 0.8% desiccated ox bile, 0.1% v/v glycerol, 0.05% w/v glycerol monostearate, 0.5% v/v Tween 60, and 2% v/v oleic acid, 1% w/v agar in distilled water) and modified Leeming and Notman agar supplemented with cyclohexamide (0.5%) and chloramphenicol (0.05%)(21), as fungal general medium and incubated at 32ºC for two weeks in the dark. The study then proceeded as follows, to identify the Malassezia species. This research was approved by the ethics committee of Mazandaran University of Medical Science and written informed consent was obtained from the each participant prior to enrolment.

2.2. Microscopic and Physiological Characteristics

Among Malassezia species, only M. pachydermatis is capable of growing on Sabouraud’s agar. However, more tests are essential for identification of the remaining Malassezia species such as Tween assimilation test, catalase reaction and splitting of esculin. After one week of incubation on modified Leeming and Notman agar at 32º C, the yeast cells were examined morphologically by gram and methylen blue staining. The catalase reaction was performed by the application of a drop of hydrogen peroxide (30% solution) onto a culture smear on a glass slide. Production of gas bubbles was considered as a positive reaction. M. restricta is the only lipid- dependent species lacking catalase (22, 23).

2.3. Splitting of Esculin

According to the method described by Mayser et al. (24), the b-glucosidase activity of different Malassezia species was assayed. Briefly, the loop of fresh yeast was deeply inoculated in the esculin agar (Merck, Germany) tube and incubated for 5 days at 32 ºC. The splitting of esculin is indicated by darkening of the medium. This test was used to distinguish M. furfur, M. slooffiae and M. sympodialis from other Malassezia species.

2.4. Tween Assimilation Test

The ability to utilize individual Tween compounds (Tween 20, 40, 60 and 80) was tested according to Guillot et al. (20). Briefly; the sterile Sabouraud's agar (16 ml) was melted and allowed to cool to approximately 50˚C. Malassezia yeast suspensions (about 105 cfu/mL) were mixed with Sabouraud's agar, and the mixtures were plated. Five holes were made in the agar by the means of a 2 mm diameter punch and filled with 5 μl of Tween 20, 40, 60 and 80 (Merck, Germany). The plates were incubated for one week at 32º C. Utilization of Tween was assessed by the degree of growth and /or reaction (precipitation) of the lipophilic yeasts around individual wells.

2.5. Statistical Analysis

Data collected in checklists were analyses using SPSS version.16. The data were analyzed using the chi-squared test. A P value of < 0.05 was considered significant.

3. Results

Of the 134 skin scraping samples, 116 patients (86.5%) were confirmed with pityriasis versicolor, based on the presence of both hyphae and spores in direct microscopy with KoH 20% and methylene blue staining, however, the Malassezia spp. were isolated from100/116 (86.2%) or 100/134 (74.6%) patients in the culture media, who were the final enrolled subjects. Table 1 shows that the distribution of patients clinically suspected of pityriasis versicolor based on age/ sex, indicating that there was no significant difference between age and gender of patients with pityriasis versicolor.

Table 1.

Distribution of Patients Clinically Suspected of pityriasis versicolor Based on Age/Sex

Age, yearsMale No. (%)Female No. (%)Total No. (%)
≤ 54 (3)3 (2.2)7 (5.2)
6 - 141 (9.7)15 (11.2)28 (20.9)
15 - 2420 (14.9)31 (23.1)51 (8.1)
25 - 3416 (11.9)21 (15.7)37 (27.6)
35 - 443 (2.2)3 (2.2)6 (4.5)
≥ 454 (3)1 (.7)5 (3.7)
Total60 (44.8)74 (55.2)134 (100)

According to descending frequency for the presence of Malassezia species among patients, M. globosa was found in n = 54; 54% cases, M. furfur in n = 32; 32% cases, M. sympodialis in n = 6; 6% cases, M. restricta in n = 6; 6% cases and M. slooffiae in n = 2; 2% cases. In this survey M. pachydermatis and M. obtusa were not found in any of the cases. There was a significant association between age and Malassezia species frequency (χ² = 36.32 df = 20, P = 0.014) (Table 2). There was no significant association between gender of patients and Malassezia species frequency (χ² = 9.24 df = 4, P = 0.055) (Table 3). Table 4 has shown the frequency of isolated Malassezia species based on anatomical locations. There was no significant association between anatomical sites and Malassezia species frequency (χ² = 23.26 df = 20, P = 0.28) (Table 4).

Table 2.

Malassezia Species Frequency According to Age of Patients (P = 0.014)

Malassezia spp.M. globosa % M. furfur % M. sympodialis %M. restricta % M. slooffiae %Total, %
Age, y
≤ 5311--5
6 - 148811119
15 - 2433922-46
25 - 3451322-22
35 - 443--1-4
≥ 4521--14
Total5432662100
Table 3.

Frequency of Malassezia Species According to Gender (P = 0.055)

M. globosa % M. furfur %M. sympodialis %M. restricta % M. slooffiae %Total, %
Male26184-250
Female281426-50
Total5432662100
Table 4.

Frequency of Malassezia Species According to the Lesion Site (P = 0.276)

M. globosa %M. furfur %M. sympodialis %M. restricta %M. slooffiae %Total ,%
Chest128---20
Back11535125
Abdomen1491-125
Neck931--13
Face7411-13
Arms13---4
Total5432662100

4. Discussion

Although, Malassezia yeasts are part of the normal flora of the skin and are discovered in 75–98% of healthy hosts, their association with various skin disorders have been established; many studies have been conducted on the distribution of these yeasts (1-3). A great number of epidemiological studies using culture or molecular-based methods, e.g. PCR-RFLP or nested-PCR, have been performed in different geographical regions in order to investigate Malassezia species in patients with pityriasis versicolor (23, 25-27), including culture-based studies carried out in Spain (25, 28, 29), Japan (26), Bosnia and Herzegovina (30) Tunisia (27), Iran (31, 32), Turkey (33) and India (34).

By using morphological and physiological characteristics particularly in tropical areas, M. globosa either alone or associated with other Malassezia spp. (e.g. M. sympodialis, M. slooffiae) was the most commonly isolated Malassezia species. This ratio that indicated the predominance of M. globosa was between 53.3% and 63.3 % (25-28, 30-35). In contrast, a study carried out by Gupta et al. (36) indicated that M. Sympodialis was the predominant pityriasis versicolor isolate (59.5%), followed by M. globosa (25.2%), M. furfur (10.8%), M. slooffiae (2.7%), M. restricta (0.9%) and M. obtusa (0.9%) in Canada. In the present study, the most predominant species observed was M. globosa (54%) followed by M. furfur (32%), M. sympodialis (6%), M. restricta (6%) and M. slooffiae (2%). Nevertheless, M. pachydermatitis and M. obtuse were not observed from pityriasis versicolor lesions.

Our findings for M. globosa were most compatible to that of other similar studies (25, 26, 28, 30-35). However, M. furfur and M. slooffiae seemed to occur more frequently than in other studies carried out in Canada (6) Spain (25, 28, 35), Japan (26) Iran (28,29), Tunusia (27) and Bosnia (25), in which a frequency between 0% and 25.3%, and 0% and 5.3% was reported , respectively. In this study, no significant differences were found in species isolated according to the clinical type or anatomical sites of lesions. In contrast, in Bosnia, Prohic et al. (30) and in Spain, Erchiga et al. (25) reported that no significant differences were found in the isolated species according to the clinical sign or anatomical sites of lesions. In this study, the recovery rate of Malassezia spp. from pityriasis versicolor lesions was 74.6 % (100/134). In similar studies, this ratio tended to vary between 43.8% and 91.3% (17, 25-28, 30-34, 37-40).

It was noted that detection of different ratios of Malassezia species in patients with pityriasis versicolor in different parts of the world could be due to the use of different culture media (Leeming–Notman and modified Dixon agar) (25), climatic regions (tropical, subtropical, etc) (41), different sampling methods (swabbing/scraping) (25) and characteristics of patients (41). Although pityriasis versicolor has worldwide occurrence, its frequency is variable and depends on different climatic, occupational and socio-economic conditions (42, 43). In high temperate areas, the disorder is common in young adults aged 17–24 years. In tropical climates, pityriasis versicolor is more common in all age groups, but most cases occur in individuals aged 10–19 years (39).

In agreement with other investigations (43, 44), the highest prevalence of pityriasis versicolor in this study was observed for those aged between 15 to 24 years old , suggesting that the peak of the infection coincided with age periods when the sebum production is atits highest level. The role of gender in propensity to development of pityriasis versicolor is still unclear (29). To date the data revealed that pityriasis versicolor affected male individuals more than females (45, 46). However, several studies indicated that the incidence was higher in women (47, 48). In this survey we did not find significant association between gender of infected patients and the frequency of Malassezia species, this may be attributable to the extra attention of both sexes to beauty and skin hygiene (22).

Lesions mostly were found in the neck, face, back, arms, abdomen, and chest and in this survey, the most affected areas were found to be the chest, back and abdomen, which is concordance with the majority of studies worldwide (17, 49). The distribution of Malassezia species on the back and chest is proportional to the density and activity of pilosebaceous glands in these areas. However, there are a few reports indicated that pityriasis versicolor lesions can occur in unusual locations such as the nipple, genital areas and groin (49, 50).

5. Conclusions

According to our data, M. globosa was the main species causing pityriasis versicolor, as it was isolated from 54% of the lesions; followed by M. furfur (32% of lesions), while M. pachydermatitis and M. obtuse were not found in any of the cases and in 13.8% (16/116) of patients the culture was negative. The results demonstrated a significant relationship between the frequency of Malassezia species and age, however, gender and anatomical site of lesions of pityriasis versicolor was not significant. However, more studies with larger samples have to be performed to clarify the investigated subject. Since Malassezia species show different responses to antifungal therapy, thus correct identification of Malassezia species and antifungal susceptibility tests could facilitate selection of appropriate antifungal agents.

Acknowledgements

References

  • 1.

    Ahn Kyu Joong. Taxonomy of the genus Malassezia. Korean J Med Mycol. 1998;3(2):81-88.

  • 2.

    Alison SK, Ann GM, Michael PH. Freed-berg IM Eisen AZ, Wolf K, Austen KF, Goldsmith LA, Katz SI, editor. Yeast infection: Candidiasis, Pityriasis (Tinea) versicolor. 2006–2018. 6 ed. McGraw-Hill, New York; 2003.

  • 3.

    Baillon Henri. Treaty fungal medical botany tracking table droguier of the Faculty of Medicine of Paris. O. Doin; 1889.

  • 4.

    McGinley KJ, Lantis LR, Marples RR. Microbiology of tinea versicolor. Arch Dermatol. 1970;102(2):168-71. [PubMed ID: 5464320].

  • 5.

    Bergbrant IM. Seborrhoeic dermatitis and Pityrosporum ovale: cultural, immunological and clinical studies. Acta Derm Venereol Suppl (Stockh). 1991;167:1-36. [PubMed ID: 1839943].

  • 6.

    Bergbrant IM, Johansson S, Robbins D, Scheynius A, Faergemann J, Soderstrom T. An immunological study in patients with seborrhoeic dermatitis. Clin Exp Dermatol. 1991;16(5):331-8. [PubMed ID: 1838969].

  • 7.

    Parunovic A, Halde C. Pityrosporum orbiculare. Its possible role in seborrheic blepharitis. Am J Ophthalmol. 1967;63(4):815-20. [PubMed ID: 4225663].

  • 8.

    Borton LK, Schwartz RA. Pityrosporum folliculitis. A common acne form condition of middle age. Arz Med. 1981;38:598-601.

  • 9.

    Kellet JK, Macdonald RH. Confluent and reticulate papillomatosis. Arch Dermatol. 1985;121(5):587-8. [PubMed ID: 3994403].

  • 10.

    Dankner WM, Spector SA, Fierer J, Davis CE. Malassezia fungemia in neonates and adults: complication of hyperalimentation. Rev Infect Dis. 1987;9(4):743-53. [PubMed ID: 3125578].

  • 11.

    Larocco M, Dorenbaum A, Robinson A, Pickering LK. Recovery of Malassezia pachydermatis from eight infants in a neonatal intensive care nursery: clinical and laboratory features. Pediatr Infect Dis J. 1988;7(6):398-401. [PubMed ID: 3134645].

  • 12.

    Mickelsen PA, Viano-Paulson MC, Stevens DA, Diaz PS. Clinical and microbiological features of infection with Malassezia pachydermatis in high-risk infants. J Infect Dis. 1988;157(6):1163-8. [PubMed ID: 3373021].

  • 13.

    Richet HM, McNeil MM, Edwards MC, Jarvis WR. Cluster of Malassezia furfur pulmonary infections in infants in a neonatal intensive-care unit. J Clin Microbiol. 1989;27(6):1197-200. [PubMed ID: 2753995].

  • 14.

    Welbel SF, McNeil MM, Pramanik A, Silberman R, Oberle AD, Midgley G, et al. Nosocomial Malassezia pachydermatis bloodstream infections in a neonatal intensive care unit. Pediatr Infect Dis J. 1994;13(2):104-8. [PubMed ID: 8190533].

  • 15.

    Francis P, Walsh TJ. Approaches to management of fungal infections in cancer patients. Oncology (Williston Park). 1992;6(5):133-44. discussion 144, 147-8. [PubMed ID: 1534671].

  • 16.

    Samonis G, Bafaloukos D. Fungal infections in cancer patients: an escalating problem. In Vivo. 1992;6(2):183-93. [PubMed ID: 1525339].

  • 17.

    Goodman DS, Teplitz ED, Wishner A, Klein RS, Burk PG, Hershenbaum E. Prevalence of cutaneous disease in patients with acquired immunodeficiency syndrome (AIDS) or AIDS-related complex. J Am Acad Dermatol. 1987;17(2 Pt 1):210-20. [PubMed ID: 2957397].

  • 18.

    Gueho E, Midgley G, Guillot J. The genus Malassezia with description of four new species. Antonie Van Leeuwenhoek. 1996;69(4):337-55. [PubMed ID: 8836432].

  • 19.

    Sugita T, Tajima M, Ito T, Saito M, Tsuboi R, Nishikawa A. Antifungal activities of tacrolimus and azole agents against the eleven currently accepted Malassezia species. J Clin Microbiol. 2005;43(6):2824-9. [PubMed ID: 15956404]. https://doi.org/10.1128/JCM.43.6.2824-2829.2005.

  • 20.

    Guillot J, Guého E, Lesourd M, Midgley G, Chévrier G, Dupont B. Identification of Malassezia species: a practical approach. J Med Mycol. 1996;6(3):103-110.

  • 21.

    Sugita T, Tajima M, Takashima M, Amaya M, Saito M, Tsuboi R, et al. A new yeast, Malassezia yamatoensis, isolated from a patient with seborrheic dermatitis, and its distribution in patients and healthy subjects. Microbiol Immunol. 2004;48(8):579-83. [PubMed ID: 15322337].

  • 22.

    Gupta AK, Kohli Y, Faergemann J, Summerbell RC. Epidemiology of Malassezia yeasts associated with pityriasis versicolor in Ontario, Canada. Med Mycol. 2001;39(2):199-206. [PubMed ID: 11346269].

  • 23.

    Marishita N, Sei Y, Sugita T. Molecular analysis of Malassezia micro flora from patients with pityriasis versicolor. Mycopatholo. 2006;161:61–65.

  • 24.

    Mayser P, Haze P, Papavassilis C, Pickel M, Gruender K, Gueho E. Differentiation of Malassezia species: selectivity of cremophor EL, castor oil and ricinoleic acid for M. furfur. Br J Dermatol. 1997;137(2):208-13. [PubMed ID: 9292068].

  • 25.

    Crespo Erchiga V, Ojeda Martos A, Vera Casano A, Crespo Erchiga A, Sanchez Fajardo F. Malassezia globosa as the causative agent of pityriasis versicolor. Br J Dermatol. 2000;143(4):799-803. [PubMed ID: 11069459].

  • 26.

    Nakabayashi A, Sei Y, Guillot J. Identification of Malassezia species isolated from patients with seborrhoeic dermatitis, atopic dermatitis, pityriasis versicolor and normal subjects. Med Mycol. 2000;38(5):337-41. [PubMed ID: 11092380].

  • 27.

    Salah SB, Makni F, Marrakchi S, Sellami H, Cheikhrouhou F, Bouassida S, et al. Identification of Malassezia species from Tunisian patients with pityriasis versicolor and normal subjects. Mycoses. 2005;48(4):242-5. [PubMed ID: 15982205]. https://doi.org/10.1111/j.1439-0507.2005.01091.x.

  • 28.

    Aspiroz C, Ara M, Varea M, Rezusta A, Rubio C. Isolation of Malassezia globosa and M. sympodialis from patients with pityriasis versicolor in Spain. Mycopathologia. 2002;154(3):111-7. [PubMed ID: 12171443].

  • 29.

    Lacaz C da S, Porto E, Martins JE Costa, Heins-Vaccari EM, Takahashi de Melo N. Treaty of medical mycology. J Ins Trop Med São Paulo. 2002;44(5):297-298.

  • 30.

    Prohic A, Ozegovic L. Malassezia species isolated from lesional and non-lesional skin in patients with pityriasis versicolor. Mycoses. 2007;50(1):58-63. [PubMed ID: 17302750]. https://doi.org/10.1111/j.1439-0507.2006.01310.x.

  • 31.

    Rasi A, Naderi R, Behzadi AH, Falahati M, Farehyar S, Honarbakhsh Y, et al. Malassezia yeast species isolated from Iranian patients with pityriasis versicolor in a prospective study. Mycoses. 2010;53(4):350-5. [PubMed ID: 19500258]. https://doi.org/10.1111/j.1439-0507.2009.01727.x.

  • 32.

    Tarazooie B, Kordbacheh P, Zaini F, Zomorodian K, Saadat F, Zeraati H, et al. Study of the distribution of Malassezia species in patients with pityriasis versicolor and healthy individuals in Tehran, Iran. BMC Dermatol. 2004;4:5. [PubMed ID: 15119958]. https://doi.org/10.1186/1471-5945-4-5.

  • 33.

    Karakas M, Turac-Bicer A, Ilkit M, Durdu M, Seydaoglu G. Epidemiology of pityriasis versicolor in Adana, Turkey. J Dermatol. 2009;36(7):377-82. [PubMed ID: 19583685]. https://doi.org/10.1111/j.1346-8138.2009.00663.x.

  • 34.

    Dutta S, Bajaj AK, Basu S, Dikshit A. Pityriasis versicolor: socioeconomic and clinico-mycologic study in India. Int J Dermatol. 2002;41(11):823-4. [PubMed ID: 12453015].

  • 35.

    Erchiga V Crespo, Martos A Ojeda, Casaño A Vera, Erchiga A Crespo, Fajardo F Sanchez, Guého E. Mycology of pityriasis versicolor. 2008.

  • 36.

    Gupta AK, Kohli Y, Summerbell RC, Faergemann J. Quantitative culture of Malassezia species from different body sites of individuals with or without dermatoses. Med Mycol. 2001;39(3):243-51. [PubMed ID: 11446527].

  • 37.

    Gaitanis G, Velegraki A, Alexopoulos EC, Chasapi V, Tsigonia A, Katsambas A. Distribution of Malassezia species in pityriasis versicolor and seborrhoeic dermatitis in Greece. Typing of the major pityriasis versicolor isolate M. globosa. Br J Dermatol. 2006;154(5):854-9. [PubMed ID: 16634886]. https://doi.org/10.1111/j.1365-2133.2005.07114.x.

  • 38.

    Gaitanis G, Velegraki A, Frangoulis E, Mitroussia A, Tsigonia A, Tzimogianni A, et al. Identification of Malassezia species from patient skin scales by PCR-RFLP. Clin Microbiol Infect. 2002;8(3):162-73. [PubMed ID: 12010171].

  • 39.

    Iskit S, Ilkit M, Turc-Bicer A, Demirhindi H, Turker M. Effect of circumcision on genital colonization of Malassezia spp. in a pediatric population. Med Mycol. 2006;44(2):113-7. [PubMed ID: 16519013].

  • 40.

    Leeming JP, Notman FH. Improved methods for isolation and enumeration of Malassezia furfur from human skin. J Clin Microbiol. 1987;25(10):2017-9. [PubMed ID: 3667925].

  • 41.

    Gupta AK, Batra R, Bluhm R, Boekhout T, Dawson TL, Jr. Skin diseases associated with Malassezia species. J Am Acad Dermatol. 2004;51(5):785-98. [PubMed ID: 15523360]. https://doi.org/10.1016/j.jaad.2003.12.034.

  • 42.

    Borelli D, Jacobs PH, Nall L. Tinea versicolor: epidemiologic, clinical, and therapeutic aspects. J Am Acad Dermatol. 1991;25(2 Pt 1):300-5. [PubMed ID: 1918469].

  • 43.

    Sunenshine PJ, Schwartz RA, Janniger CK. Tinea versicolor. Int J Dermatol. 1998;37(9):648-55. [PubMed ID: 9762812].

  • 44.

    Midgley G, Gueho E, Guillot J. Disease caused by Malassezia species. 4. 9 ed. London: Arnold; 1998.

  • 45.

    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(5):323-9. [PubMed ID: 1955952].

  • 46.

    Prohic A. Identification of Malassezia species isolated from scalp skin of patients with psoriasis and healthy subjects. Acta Dermatovenerol Croat. 2003;11(1):10-6. [PubMed ID: 12718790].

  • 47.

    Gupta AK, Bluhm R, Summerbell R. Pityriasis versicolor. J Eur Acad Dermatol Venereol. 2002;16(1):19-33. [PubMed ID: 11952286].

  • 48.

    Nikpoor N, Buxton MW, Leppard BJ. Fungal diseases in Shiraz. Pahlavi Med J. 1978;9(1):27-49. [PubMed ID: 148630].

  • 49.

    Rudolph RI, Holzwanger JM. Letter: Inverse tinea versicolor. Arch Dermatol. 1975;111(9):1213. [PubMed ID: 1167054].

  • 50.

    Burkhart CG, Dvorak N, Stockard H. An unusual case of tinea versicolor in an immunosuppressed patient. Cutis. 1981;27(1):56-8. [PubMed ID: 7009073].