Black fungal extremes - CBS

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Ti n e a n i g r aand Polynesia (Uezato et al. 2006). The disorder is rare in Europe(Hughes et al. 1993, Reid 1998) and the United States (Burke1993, Shanon et al. 1999, Tseng et al. 1999). Predisposing factorsassociated with the condition are hyperhydrosis (Severo et al.1994, Bonifaz 2001, Padilla et al. 2002) and presence in coastalsee areas or hypersaline environments, where the causative agentmay be picked up from the natural habitat (de Hoog & Gerrits vanden Ende 1992).Our 22 cases present a large series and, unlike other publishedreports (for example, Severo et al. 1994, Perez et al. 2005), cover along follow-up period. Our cases are clinically and demographicallysimilar to the ones reported from other continents (Uezato et al.2006). Tinea nigra is considered a rare disease. According tostatistics in our hospital in Mexico City, D.F., it accounts for 0.085% of all mycoses. The frequency of the disorder may be higher, butdue to its asymptomatic nature and the possibility of spontaneouscure, patients seldom reach the doctor’s office. This is the case onlywhen patients worry because of confusion with other pigmentedskin diseases, such as melanoma.The disorder has no preference for age categories (Table 1),cases equally occurring in adults and children, and no genderdifferences are observed (Durán et al. 1993, Pegas et al. 2003).Course of the infection according to our data was 1−18 mos, witha mean incubation time of 3.8 mos. According to the patient’sinformation, we think that the developing lesions become visiblewithin 15–30 ds. The lesions are invariably flat, not elevatedand without inflamed margins; they consist of pigmented, mostlybrownish, irregular and asymptomatic macules and with welldefinedborders, and are covered by fine scaling. Some patientsFig. 3. Culture of Hortaea werneckii on SGA. Two phases: yeast-like phase withmoist colonies, and filamentous colony (case 11, CBS 122344; Table 1).Fig. 4. Multiple blastoconidia with central septa (KOH, 40×). (case 20, CBS 122342;Table 1).report that throughout the day a change in colour of the maculescan be observed: early in the morning macules can appear in moreintense pigmentations but they fade as the day goes by. This isprobably due to the fact that the fungus is cleared from the hands asa result of daily activities. Only one patient in our study, presentedwith erythema, also reported moderate itching as was noted inother studies (Hughes et al. 1993, Perez et al. 2005).Tinea nigra has a major clinical relevance because it can bemistaken for various types of nevi. In some reports it even wasmisidentified as melanomas. Also some of our cases, seen atexternal dermatology services, were initially diagnosed as varioustypes of nevi (Hall & Perry 1998, Tseng et al. 1999). With thisincorrect diagnosis, two of the cases underwent biopsies, whichlead to the observation of fungal elements in the stratum corneumwith a discrete perivascular infiltrate. Differential diagnosis isessential, due to the extremely different prognosis of the variousconditions. The tinea nigra macule denotes the superficial growthof the fungus, strictly limited to the stratum corneum. This maybe revealed by dermatoscopy, which is a technique allowing theobservation of fungal elements with certainty, particularly whenflanked with microbiological tests (Smith et al. 2001; Fig. 2F).The palms of hands constitute the major location of the disease,which explains the often-used name “tinea nigra palmaris”. Mostcases are unilateral but also bilateral infections can be observed(Tseng et al. 1999), probably resulting from autoinoculation (Fig.2A). In our study, in 19/22 cases the disorders were located on thepalms and 3 on the soles. Surprisingly, one of the sole infectionswas located in the interdigital spaces (Fig. 2E) and had a discretepigmentation (case 13, strain CBS 123045; see Table 1), which ledto suspect dermatosis neglecta caused by the chronic deposition ofdirt or filth (Ruiz-Maldonado et al. 1999). We are unaware of anycase of a tinea nigra located in the interdigital spaces. Recentlya similar condition caused by chaetothyrialean black yeast-likefungi was reported (Badali et al. 2008), differing by the fact that theetiologic fungus concerned, Cladophialophora saturnica showedinvasive behaviour, while Hortaea werneckii is strictly commensal.The two cases located on the plantar region were also informative,as they concerned patients with the habit of running barefootalong the seaside, an environment with high salinity and probablythe natural niche of the fungus. Both cases had a clinical historyof hyperhydrosis probably resulting in saline plantar cutaneousconditions and adhesion of the fungus (Fig. 2C; Göttlich et al.1995). It is important to comment on case 16 (Table 1), an irregularworker in saltpans, that is considered the natural enviroment ofH. werneckii. It is probable that more saltpan-workers carry thedisorder but due to the asymptomatic nature of the disease do notseek medical help (Gunde-Cimerman et al. 2000).Recently Ng et al. (2005) reported the isolation of H. werneckiifrom the serum and a splenic abscess of a human patient. Thisis an exceptional case, in which the fungus behaved as anopportunistic pathogen and was the causative agent of a systemicphaeohyphomycosis.Given the taxonomic uncertainties mentioned above,confirmation of identification with microbiological and moleculartests is compulsory. Direct KOH examinations provide us with quickinformation and demonstrate the short, tortuous, thick, light brownhyphae, which may occasionally be darkened, and sometimespresent short filaments and yeast-like cells. The pigmentation ofhyphae unambiguously distinguishes tinea nigra from variousother types of dermatophytoses or skin infections (Hughes et al.1993, Gupta et al. 2003). The use of chlorazol black (Feuilhade deChauvin 2005) as a clearing solution is not recommended becausewww.studiesinmycology.org81
Bo n i fa z e t a l.this reagent stains fungal elements black, which interferes withdistinction from dermatophyte hyphae. In our study nearly all caseswere diagnosed by direct examination and were confirmed byculture. Colonies of Hortaea werneckii grow on a standard mediawithin 5–8 ds. They are initially black with a creamy appearanceand later become filamentous. This morphological transition ischaracteristic for H. werneckii, but is also known in Exophiala(Chaetothyriales). Filamentous isolates may be mistaken for somechaetothyrialean fungi or for Cladosporium spp. Conidia appear aspigmented yeast cells with a dark central septum, the outer walllater becoming thick-walled, heavily pigmented. Conidia finallygerminate with hyphae resulting in yeast-like colonies that graduallychange over into filaments to complete the anamorph life cycle.Molecular diagnostics of H. werneckii were developed byUijthof et al. (1994) using PCR-fingerprinting techniques and byZalar et al. (1999) using sequencing of rDNA ITS. Uezato et al.(1989) applied molecular diagnostics in clinical practice. Abliz etal. (2003) developed specific primers on the basis of ITS data andvalidated the primers by a comparison with 42 other melanizedfungal species, including chaetothyrialean agents of cutaneous andsubcutaneous disease.The treatment of tinea nigra is very simple and effective. Mostcases resolve with only keratinolytic agents like urea, salicylicacid and Whitfield ointment, applied once or twice a day (Sayegh-Carreno et al. 1989, Bonifaz 2001). Most of the cases in ourreport were managed with Whitfield ointment. Mean treatmentduration (Table 2) was approximately 15 ds; two cases presentedspontaneous cure. Most topical antifungals are also effective. Goodtreatment results have been reported using miconazole (Markset al. 1980), ketoconazole (Chang & Arenas 1983, Burke 1993),bifonazole (Meisel 1984), terbinafine (Shanon et al. 1999) andciclopirox olamine (Rossen & Lingappan. 2006). There is even areport of oral itraconazole therapy (Gupta et al. 1997), which is notrecommended for this commensal fungus. Most cases in our studyresolved with topical therapy within two weeks.REFERENCESAbliz P, Fukushima K, Takizawa K, Miyaji M, Nishimura K (2003). Specificoligonucleotide primers for identification of Hortaea werneckii, a causativeagent of tinea nigra. Diagnostic Microbiology and Infectious Diseases 46:89–93.Anomymous (2004). Guidelines. Classification of organisms – Fungi. Swiss Agencyfor the Environment, Forests and Landscape.Badali H, Carvalho VO, Vicente V, Attili-Angelis D, Kwiatkowski IB, Gerrits vanden Ende AHG, Hoog GS de (2008). Cladophialophora saturnica sp. nov., anew opportunistic species of Chaetothyriales revealed using molecular data.Medical Mycology 7: 1–12.Bonifaz A (2001). Tinea nigra. In Arenas R, Estrada R (eds): Handbook of TropicalDermatology. Landes Bioscience eds. Georgetown, Texas: 24–26.Burke WA (1993). Tinea nigra: treatment with topical ketoconazole. Cutis 52: 209–211.Chang P, Arenas R (1983). Tiña negra palmar tratada con ketoconazol. DermatologíaRevista Mexicana 27: 218–219.Crous PW, Braun U, Groenewald JZ (2007a). Mycosphaerella is polyphyletic. Studiesin Mycology 58: 1–32.Crous PW, Braun U, Schubert K, Groenewald JZ (2007b). Delimiting Cladosporium frommorphologically similar genera. Studies in Mycology 58: 33−56.Durán C, Carbajosa J, Arenas R (1983). Tiña negra plantar. Estudio de tres casos enMéxico. (1993). Dermatología Revista Mexicana 36: 170–171.Feuilhade de Chauvin M (2005). New diagnostic techniques. Journal of EuropeanAcademy Dermatology and Venereology 19, Suppl. 1: 20–24.Göttlich E, Hoog GS de, Yoshida S, Takeo K, Nishimura K, Miyaji M (1995). Cellsurface hydrophobicity and lipolysis as essential factors in human tinea nigra.Mycoses 38: 489–494.Gunde-Cimerman N, Zalar P, Hoog GS de, Plemenitas A (2000). Hypersalinewaters in salterns: natural ecological niches for halophilic black yeasts. FEMSMicrobiological Ecology 32: 235−240.Gupta AK, Chaudhry M, Elewski B (2003). Tinea corporis, tinea cruris, tinea nigra,and piedra. Dermatologia Clinica 21: 395–400.Gupta G, Burden AD, Shankland GS, Fallowfield ME, Richardson MD (1997). Tineanigra secondary to Exophiala werneckii responding to itraconazole. BritishJournal of Dermatology 137: 483–484.Hall J, Perry VE (1998). Tinea nigra palmaris: differentiation from malignant melanomaor junctional nevi. Cutis 62: 45–46.Hoog GS de, Gerrits van den Ende AHG (1992). Nutritional pattern and ecophysiologyof Hortaea werneckii, agent of human tinea nigra. Antonie vanLeeuwenhoek 62: 321–329.Hoog GS de, Guarro J, Gené J, Figueras MJ (2000). Atlas of Clinical Fungi, 2 nd ed.Centraalbureau voor Schimmelcultures / Universitat Rovira i Virgili, Utrecht /Reus.Hughes JR, Moore MK, Pembroke AC (1993). Tinea nigra palmaris. Clinical andExperimental Dermatology 18: 481–483.Kogej T, Stein M, Volkmann M, Gorbushina AA, Galinski EA, Gunde-Cimerman N (2007).Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytesand melanization. Microbiology 153: 4261–4273.Marks JG, King RD, Davis BM (1980). Treatment of tinea nigra palmaris with miconazoletopically. Archives of Dermatology 116: 321–322.McGinnis MR, Schell WA, Carson J (1985). Phaeoannellomyces and thePhaeococcomycetaceae, new dematiaceous blastomycete taxa. Sabouraudia23: 179–188.Meisel C (1984). Treatment of tinea palmaris with Mycospor. Dermatologica 169,Suppl. 1: 121-123.Ng KP, Soo-Hoo TS, Na SL, Tay ST, Hamimah H, Lim PC, Chong PP, Chavez AJ,Messer SA (2005). The mycological and molecular study of Hortaea werneckiiisolated from blood and splenic abscess. Mycopathologia 159: 495–500.Padilla MC, Medina CD, Eng A, Alonzo L (2002). Tiña negra. Presentación de uncaso. Revista Centro Dermatológico Pascua 11: 139–141.Pegas JR, Criado PR, Lucena SK, de Oliveira MA (2003). Tinea nigra: report of twocases in infants. Pediatrics Dermatology 20: 315–317.Perez C, Colella MT, Olaizola C, Hartung de Capriles C, Magaldi S, Mata-EssayagS (2005). Tinea nigra: report of twelve cases in Venezuela. Mycopathologia160: 235–238.Petrovic U (2006). Role of oxidative stress in the extremely salt-tolerant yeastHortaea werneckii. FEMS Yeast Research 6: 16–22.Plemenitaš A, Vaupotič T, Lenassi M, Kogej T, Gunde-Cimerman N (2008).Adaptation of extremely halotolerant black yeast Hortaea werneckii toincreased osmolarity: a molecular perspective at a glance. Studies in Mycology61: 67-75.Reid BJ (1998). Exophiala werneckii causing tinea nigra in Scotland. British Journalof Dermatology 139: 157–158.Rosen T, Lingappan A (2006). Rapid treatment of tinea nigra palmaris with cilopiroxolamine gel, 0.77 %. Skinmed 5: 201–203.Ruiz-Maldonado R, Duran-McKinster C, Tamayo-Sanchez L, Orozco-CovarrubiasML (1999). Dermatosis neglecta: dirt crusts simulating verrucous nevi. Archivesof Dermatology 135: 728–729.Sayegh-Carreno R, Abramovits-Ackerman W, Giron GP (1989). Therapy of tineanigra plantaris. International Journal of Dermatology 28: 46–48.Severo LC, Bassanesi MC, Londero AT (1994). Tinea nigra: report of four casesobserved in Rio Grande do Sul (Brazil) and a review of Brazilian literature.Mycopathologia 126: 157–162.Shannon PL, Ramos-Caro FA, Cosgrove BF, Flowers FP (1999). Treatment of tineanigra with terbinafine. Cutis 64: 199–201.Smith SB, Beals SL, Elston DM, Meffert JJ (2001). Dermoscopy in the diagnosis oftinea nigra plantaris. Cutis 68: 377–380.Tseng SS, Whittier S, Miller SR, Zalar GL (1999). Bilateral tinea nigra plantaris andtinea nigra plantaris mimicking melanoma. Cutis 64: 265–268.Uezato H, Gushi M, Hagiwara K, Kayo S, Hosokawa A, Nonaka S (1989). A case oftinea nigra palmaris in Okinawa, Japan. Journal of Dermatology 33: 23–29.Uijthof JM, Cock AW de, Hoog GS de, Quint WG, Belkum A van (1994). Polymerasechain reaction-mediated genotyping of Hortaea werneckii, causative agent oftinea nigra. Mycoses 37: 307–312.Zalar P, Hoog GS de, Gunde-Cimerman N (1999). Ecology of halotolerantdothideaceous black yeasts. Studies in Mycology 43: 38–48.82
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Studies in Mycology 61 (2008)Black
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Studies in MycologyThe Studies in M
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PREFACEThe terms "black fungi" or "
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Dr o u g h t m e e t s a c i dTable
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Dr o u g h t m e e t s a c i d2003/
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Za l a r e t a l.Table 1. List of a
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Za l a r e t a l.Table 1. (Continue
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Origin o f Ex o p h i a l a d e r m
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Bi o d i v e rs i t y o f t h e g e
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homogentisate 165, 171, 173Hortaea
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CBS Biodiversity SeriesNo. 6: Alter
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Studies in Mycology (ISSN 0166-0616
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Satow MM, Attili-Angelis D, Hoog GS
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