Medical Mycology June 2004, 42, 273 /276
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 typical
fingernail 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 macroconidia 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 of T. raubitschekii have been reported in the
literature [2 /5] and although a definite worldwide
profile of the epidemiological and clinical aspects of
such isolates is still lacking, this dermatophyte seems to
Received 27 June 2003; Accepted 10 July 2003
Correspondence: Manuela Papini (MD): Viale degli Oleandri 62,
05100 Terni, Italy. Tel.: /39 0744 404781; Fax: /39 0744 205385;
E-mail: [email protected]
– 2004 ISHAM
have a strong connection with patients who have
resided in an Asian or African country. Onychomycosis
caused by T. raubitschekii- like isolates has been reported 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.
DOI: 10.1080/13693780310001602794
274
Papini et al.
Case report and mycology
A 22-year-old black male student from Cameroon
presented to the outpatient service of Terni Dermatological 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 a
volunteer 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 cycloheximide 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 pencilshaped macroconidia and club-like to pyriform microconidia (Fig. 3); rounded inflated cells were occasionally seen. Scanning electron microscope examination of
the colonies clearly showed masses of cylindrical
macroconidia as well as pedicellate microconidia produced along the hyphae (Fig. 4). Bromcresol purple,
Fig. 1
Isolate colonies after 10 days on Sabouraud glucose agar.
Fig. 2
Reverse side of the colonies showing red-brown pigmentation.
milk-solids yeast-extract agar showed restricted colonial growth without colour change of the indicator
within 14 days. The urease test on Christensen urea
broth was strongly positive after 5 days. Hair perforation was negative. These macroscopic and microscopic
aspects of the isolate and its cultural behaviour allowed
the identification of T. 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. 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
T. raubitschekii onychomycosis
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 .
Discussion
The epidemiology and the clinical manifestations of
dermatophyte infections in Europe have clearly changed 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 in
cases caused by anthropophilic fungi such as T.
violaceum, T. soudanense, T. tonsurans and M. audouinii , 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 experiences of Taplin [11], who found that ringworm in
Vietnamese adults was nearly always caused by T.
– 2004 ISHAM, Medical Mycology, 42, 273 /276
275
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 characteristics 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 underrecognized. 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 misidentification. A better awareness of this phenotype can
probably increase its correct recognition, adding epidemiological data of great importance to the understanding 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. raubitschekii cannot currently be used as a recognized
species name, but correct laboratory reports can be
issued making information about this phenotype accessible and allowing report recipients to do comprehensive 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 Biodiversity Centre, Utrecht, the Netherlands, for his assistance
in confirming the identification of the T. raubitschekii
phenotype.
References
1 Kane J, Salkin IF, Weitzman I, Smitka C. Trichophyton raubitschekii sp. nov. Mycotaxon 1981; 13: 259 /266.
2 Kane J, Krajden S, Summerbell RC, Sibbald RG. Infections
caused by Trichophyton raubitschekii : clinical and epidemiological
features. Mycoses 1990; 33: 499 /506.
3 Caiuby MJ, Monteiro PC, Nishikawa MM. Isolation of Trichophyton raubitschekii in Rio de Janeiro (Brazil). J Med Vet Mycol
1996; 34: 361 /363.
276
Papini et al.
4 Lacaz CZ, Zaitz C, Ruiz LR, et al . Dermatophytosis caused by
Trichophyton raubitschekii . Report of the first case in São Paulo,
Brazil. Rev Inst Med Trop São Paulo 1999; 41: 313 /317.
5 Tietz HJ, Hopp M, Gräser Y. First isolation of Trichophyton
raubitschekii (syn. T. rubrum ) in Europe. Mycoses 2002; 45: 10 /
14.
6 Summerbell RC, Haugland RA, Li A, Gupta AK. rRNA gene
internal transcribed spacer 1 and 2 sequences of asexual,
anthropophilic dermatophytes related to Trichophyton rubrum . J
Clin Microbiol 1999; 37: 4005 /4011.
7 Gräser Y, Kuijpers AFA, Presber W, de Hoog GS. Molecular
taxonomy of the Trichophyton rubrum complex. J Clin Microbiol
2000; 38: 3329 /3336.
8 Romano C, Massai L, Difonzo E. Dermatophytosis due to
Trichophyton violaceum in Tuscany from 1985 to 1997. Mycoses
2000; 43: 169 /167.
9 Hay RJ, Robles W, Midgley G, Moore MK. European Confederation of Medical Mycology Working Party of Tinea Capitis.
Tinea capitis in Europe: a new perspective on an old problem. J
Eur Acad Dermatol Venereol 2001; 15: 229 /233.
10 Mohrenschlager M, Seidl HP, Ginter-Hanselmayer G, Abeck D.
Tinea capitis of childhood: incidence and pathogenetic role of
Trichophyton tonsurans in Central Europe. J Am Acad Dermatol
2001; 45: 320 /321.
11 Taplin D. Dermatophytosis in Vietnam. Cutis 2001; 67(Suppl. 5):
19 /20.
12 Summerbell RC, Kane J. The genera Trichophyton and Epidermophyton . In: Kane J, Summerbell RC, Sigler L, Krajden S, Land
G (eds). Laboratory Handbook of Dermatophytes. Belmont, CA:
Star Publishing Company, 1997: 131 /191.
– 2004 ISHAM, Medical Mycology, 42, 273 /276