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    Case Report

    Onychomycosis caused by an isolate conforming to the

    description of Trichophyton raubitschekii

    MANUELA PAPINI, CONSUELO GRECO & FERRUCCIO PILERI

    Perugia University, Terni Dermatological Clinic, Terni, Italy

    Trichophyton raubitschekii is currently regarded as a synonymous name betokening

    a variant form of Trichophyton rubrum . Nonetheless, isolates conforming to this

    morphotaxonomic concept have morphological, physiological and clinical features

    very different from those of typical T. rubrum . Isolates are mainly obtained from

    subjects originating from certain tropical and subtropical countries, and are mainly

    obtained from upper body skin infections, rarely from onychomycosis. In this

    paper the authors report the first known Italian case of onychomycosis caused by

    such an isolate. The patient, a male student from Cameroon, had a typicalfingernail tinea unguium, without any other sign of skin or nail infection. T.

    raubitschekii was identified on morphological and physiological grounds by the

    following features: velvety colony surface, brownish pigment, abundant macro-

    conidia and microconidia, and positive urease activity. Such isolates may prove

    very difficult to identify correctly, especially in areas like Italy where T. rubrum is

    normally seen only as isolates presenting a strongly differing phenotype.

    Keywords epidemiology, onychomycosis, taxonomy, Trichophyton raubitschekii

    Introduction

    Trichophyton raubitschekii was described as a species

    morphologically and physiologically distinct from the

    related T. rubrum by Kane et al. [1] in 1981. It was later

    shown to have strong statistical differences from typical

    T. rubrum in the spectrum of diseases it caused, in that

    it was associated strongly with tinea corporis and tinea

    cruris, only weakly with tinea pedis, and rarely with

    tinea unguium [2]. T. rubrum , by contrast, was mainly

    obtained from tinea pedis and tinea unguium. Up to

    now only 47 cases caused by isolates conforming to the

    description ofT. raubitschekii have been reported in the

    literature [2/5] and although a definite worldwideprofile of the epidemiological and clinical aspects of

    such isolates is still lacking, this dermatophyte seems to

    have a strong connection with patients who have

    resided in an Asian or African country. Onychomycosis

    caused by T. raubitschekii-like isolates has been re-

    ported in only three cases so far. In recent years,

    molecular studies have suggested that T. raubitschekii is

    genetically too close to T. rubrum to be maintained as a

    separate species; for example, it is identical in nuclear

    ribosomal internal transcribed spacer (ITS) sequence

    with T. rubrum [6,7]. Nonetheless, as T. raubitschekii

    presents a very distinct laboratory identification profile

    and is connected with differing epidemiological data,

    there is clearly still value in reporting new clinical

    information about this phenotype. Indeed, the author

    who formally synonymized T. raubitschekii with T.rubrum after molecular study, has already done so in

    connection with a German case [5].

    In the present paper, a case of thumbnail infection

    caused by an isolate conforming with T. raubitschekii is

    presented and the differential morphological and

    cultural aspects of this dermatophyte phenotype are

    briefly summarized.

    Correspondence: Manuela Papini (MD): Viale degli Oleandri 62,

    05100 Terni, Italy. Tel.: '/39 0744 404781; Fax: '/39 0744 205385;

    E-mail: [email protected]

    Received 27 June 2003; Accepted 10 July 2003

    2004 ISHAM DOI: 10.1080/13693780310001602794

    Medical Mycology June 2004, 42, 273/276

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    Case report and mycology

    A 22-year-old black male student from Cameroon

    presented to the outpatient service of Terni Dermato-

    logical Clinic, Terni, Italy, with a 2-year history of

    thumbnail alteration. The patient had attended the

    Perugia University School of Medicine for 4 years, but

    paid regular visits to Cameroon, where he served as avolunteer social worker in a hospital.

    The right thumbnail was destroyed in its distal

    portion and the remaining nail plate had an irregularly

    cracked margin. The denuded nail bed showed mild

    erythema and fine scaling. A complete examination

    failed to reveal additional infected finger- or toenails or

    any other sign of disease affecting the skin or hair.

    Microscopic examination of scales from the nail bed

    and nail plate clarified with 40% KOH revealed fungal

    hyphae. Culture test performed on Sabouraud dextrose

    agar with and without chloramphenicol and cyclohex-

    imide showed multiple velvety pinkish colonies.

    Mycological evaluation of the isolate

    After 10 days on Sabouraud dextrose agar at 258C the

    isolate produced velvety to finely granular colonies with

    a diameter of about 20 mm. The upper surface of the

    colonies showed a central low, button-shaped, folded

    elevation and a faint pinkish colour (Fig. 1); the reverse

    was blood-red to brown (Fig. 2). Microscopically, the

    isolate was characterized by abundant cigar- to pencil-

    shaped macroconidia and club-like to pyriform micro-

    conidia (Fig. 3); rounded inflated cells were occasion-

    ally seen. Scanning electron microscope examination ofthe colonies clearly showed masses of cylindrical

    macroconidia as well as pedicellate microconidia pro-

    duced along the hyphae (Fig. 4). Bromcresol purple,

    milk-solids yeast-extract agar showed restricted colo-nial growth without colour change of the indicator

    within 14 days. The urease test on Christensen urea

    broth was strongly positive after 5 days. Hair perfora-

    tion was negative. These macroscopic and microscopic

    aspects of the isolate and its cultural behaviour allowed

    the identification ofT. raubitschekii. R. Summerbell (of

    the Centraalbureau voor Schimmelcultures, Utrecht,

    The Netherlands) confirmed the identification and the

    culture was deposited as CBS 102856.

    The patient was prescribed oral terbinafine 250 mg/

    day and ciclopiroxolamine nail lacquer for 8 weeks. A

    complete recovery was obtained in 3 months and no

    relapse was observed at follow-up after 6 and 12

    months.

    Fig. 1 Isolate colonies after 10 days on Sabouraud glucose agar.

    Fig. 2 Reverse side of the colonies showing red-brown pigmentation.

    Fig. 3 Microscopic aspect, showing a typical mix of different

    conidial forms, including macroconidia, globose inflated cells and

    clavate microconidia ()/400 objective).

    2004 ISHAM, Medical Mycology, 42, 273/276

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    Discussion

    The epidemiology and the clinical manifestations of

    dermatophyte infections in Europe have clearly chan-

    ged over the last decade. After a relatively stable period

    of approximately 30 years, in which scalp infections

    caused by Microsporum canis and foot and nail

    infections by T. rubrum were the most frequent

    dermatophytoses, there are now numerous reports of

    infections caused by unusual or exotic species [8/10]. A

    large survey of tinea capitis conducted among 19

    European countries [9] has shown a clear increase incases caused by anthropophilic fungi such as T.

    violaceum, T. soudanense, T. tonsurans and M. audoui-

    nii, in particular among urban populations and in

    immigrants from Africa and the Caribbean. Now, an

    apparently more rare dermatophyte type is being

    introduced (i.e., isolates phenotypically corresponding

    to T. raubitschekii). The first case reported in Europe

    was recently reported from Germany [5]; the case

    presented in the present paper is the first report of

    nail mycosis caused by T. raubitschekii in Italy.

    Of the 47 T. raubitschekii cases reported in the

    literature, 32 involved immigrants from or residents of

    subtropical and tropical areas such as China, Vietnam,

    central Africa, and Brazil. The most common clinical

    manifestation associated with this phenotype was tinea

    corporis, seen in 25 of the recorded cases. Similar

    clinical and epidemiological observations have emerged

    from the recently summarized Vietnam war-era experi-

    ences of Taplin [11], who found that ringworm in

    Vietnamese adults was nearly always caused by T.

    raubitschekii-like isolates producing a chronic, scaly,

    dry rash generally confined to the waist. A case of

    extensive tinea corporis in a Vietnamese immigrant is

    described in detail by Kane et al. [2]. In the laboratory,

    the most readily recognizable phenotypic characteris-

    tics distinctive of the T. raubitschekii phenotype are its

    velvety to granular surface, blood-red to brownish

    pigmentation of colonies, abundant formation of

    macroconidia, and positive urease test.

    Until now T. raubitschekii has been considered a

    rare dermatophyte variant, but some considerations

    suggest that this phenotype may have been under-

    recognized. First, the colonies may show a superficial

    resemblance to more common species such as T.

    rubrum and T. mentagrophytes or even to T. violaceum

    [12]. Also, some microbiological laboratories identify

    dermatophyte isolates on the basis of macro- and

    microscopic aspects of the colonies without performing

    specific test reactions such as the urease test. These

    practices, coupled with poor knowledge of the T.raubitschekii phenotype, can easily lead to misidentifi-

    cation. A better awareness of this phenotype can

    probably increase its correct recognition, adding epide-

    miological data of great importance to the under-

    standing of the clinical relevance and geographic

    distribution of this form. It should be noted that an

    identification of such an isolate as T. rubrum is by no

    means wrong, but rather is deficient in failing to convey

    clinical and laboratory information that may be useful

    or epidemiologically interesting. The name T. rau-

    bitschekii cannot currently be used as a recognized

    species name, but correct laboratory reports can be

    issued making information about this phenotype ac-cessible and allowing report recipients to do compre-

    hensive Medline searching (e.g., by using wording such

    as T. rubrum , Afro-asiatic variant previously known as

    Trichophyton raubitschekii).

    Acknowledgements

    We thank Richard Summerbell, CBS Fungal Biodiver-

    sity Centre, Utrecht, the Netherlands, for his assistance

    in confirming the identification of the T. raubitschekii

    phenotype.

    References

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    bitschekii sp. nov. Mycotaxon 1981; 13: 259/266.

    2 Kane J, Krajden S, Summerbell RC, Sibbald RG. Infections

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    3 Caiuby MJ, Monteiro PC, Nishikawa MM. Isolation of Tricho-

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    Fig. 4 Scanning electron microscopy showing fertile hyphae with

    macro- and microconidia ()/3000 objective), in a report from Italy of

    onychomycosis caused by an isolate conforming to the description of

    Trichophyton raubitschekii.

    2004 ISHAM, Medical Mycology, 42, 273/276

    T. raubitschekii onychomycosis 275

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