Mycopathologia (2021) 186:399–409

https://doi.org/10.1007/s11046-021-00542-4 (0123456789().,-volV)
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ORIGINAL ARTICLE

Epidemiology of Dermatophytes in Belgium: A 5 Years’

Survey
Rosalie Sacheli . Lize Cuypers . Laurence Seidel . Rajae Darfouf .
Caroline Adjetey . Katrien Lagrou . Marie-Pierre Hayette

Received: 19 August 2020 / Accepted: 15 March 2021 / Published online: 26 April 20212021
Ó The Author(s), under exclusive licence to Springer Nature B.V. 2021, corrected publication 2021

Abstract Dermatophytes are among the most com-
mon fungal agents causing superficial skin infections
worldwide. Epidemiology of these infections is evolv-
ing and variable in every country. This report presents
the Belgian epidemiological data regarding the distri-
bution of dermatophytes species isolated by the two
national reference centers for mycosis during a period
of 5 years (2012–2016). Trichophyton rubrum was the
most frequently isolated species, considering all
sampling sites (60.3% on average between 2012 and
2016). More precisely, this dermatophyte was the
major agent of Tinea unguium and Tinea corporis
during this period, followed by species of the
Trichophyton mentagrophytes complex. Moreover,
Microsporum audouinii was the main etiological
agent of Tinea capitis (TC) with a frequency of
Handling Editor: J.-P. Bouchara.
R. Sacheli (&)  R. Darfouf  C. Adjetey  M.-P. Hayette
Department of Clinical Microbiology, Belgian National
Reference Center, University Hospital of Liege, Liège,
Belgium
e-mail: R.sacheli@chuliege.be
L. Seidel
Department of Biostatistics, University Hospital of Liege,
Liege, Belgium
L. Cuypers  K. Lagrou
Laboratory of Clinical Bacteriology and Mycology,
Belgian National Reference Center, University Hospital
of Leuven, Leuven, Belgium
52.5% on average between 2012 and 2016. Other
African dermatophytes species such as Trichophyton
soudanense and Trichophyton violaceum were also
agents of TC with a respective prevalence of 11.6%
and 11.5% on average. This study highlights a
different dermatophyte distribution in Belgium in
comparison with other European countries.
Keywords Dermatophytes  Epidemiology  Tinea
capitis  Onychomycoses
Introduction
Dermatophytosis is characterized by the infection of
keratinized tissues such as the skin, hair and nails. This
disease is estimated to affect more than 20–25% of the
world’s population and its incidence is constantly
rising [1, 2]. Forty different species of dermatophytes
have been described and approximately half of them
cause the majority of human infections. They are from
zoophilic, anthropophilic or environmental origin and
belong to nine clades following the newly proposed
taxonomy; Trichophyton, Epidermophyton, Nan-
nizzia, Microsporum, Lophophyton, Arthroderma,
Paraphyton, Guarromyces and Ctenomyces [3, 4].
The epidemiology of dermatophyte infections is
changing due to immigration, travel, socioeconomic
development or erroneous treatments [5]. In the past
decades, important changes in the epidemiological

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pattern of dermatophyte infections have occurred in
Europe, including Belgium. In 2002, an increase in the
number of cases of Tinea capitis (TC) due to
anthropophilic species has been reported in Brussels,
probably due to an increased immigration from Africa
in 2001 concentrated in big cities as reported by Phalet
et al. [6, 7] and Kolivras et al. [6, 7]. To date, there are
no reports of the distribution of dermatophytes in
Belgium except the annual reports of the national
reference centers for mycosis [8]. The present labo-
ratory-based retrospective study focuses on the species
distribution of dermatophyte infections in Belgium
within a 5-year period (2012–2016). This study was
set up to present an updated review on local epidemi-
ology and clarify possible trends.
Methods
Culture and Morphological Identification
This study was based on a retrospective data analysis
obtained from records of the mycology laboratory of
the University Hospital of Liège (CHU Liege) and the
University Hospitals Leuven (UZ Leuven) from 2012
January 1st to 2016 December 31. The dataset includes
samples sent from external centers to one of the two
National Reference Centers (NRC) for Mycosis as
well as samples from the patient populations attending
UZ Leuven and CHU Liège. Positive cultures, skin
scales, nail and hair fragments sent to the NRC were
collected from patients with suspected dermatomyco-
sis and referred to either the NRC of CHU Liège or UZ
Leuven. Samples that were positive for dermatophytes
during the study period were selected. For hair, skin
and nail samples, histological examination was per-
formed with Periodic Acid-Schiff (PAS) staining.
Calcofluor staining was applied at UZ Leuven. This
was followed by culture on Sabouraud glucose agar
containing chloramphenicol with and without cyclo-
heximide (bioMérieux, France) with incubation at
28 °C ± 2 °C for 3 weeks. Fungal growth was
checked every week. Macroscopic and microscopic
identification were based on colony features using
reference books [9]. Subcultures on Takashio medium
(Sabouraud diluted medium, Tritium, The Nether-
lands) were performed in the absence of sporulation.
Microscopic examination was performed using the
‘‘flag’’ method, which consists of applying a
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Mycopathologia (2021) 186:399–409
cellophane tape on the surface of culture, followed
by adding lactophenol blue (Roth, Belgium).
As this study was based on laboratory records, it
was difficult to distinguish among relapses relative to
specimens received from the same patient. Therefore,
the number of specimens was not corrected for
duplicates.
Molecular Identification
When the identification with conventional methods was
doubtful, ITS sequencing was performed from cultures in
Sabouraud broth (Merck, Germany) [10]. Briefly at CHU
Liège, DNA was extracted from the mycelial mass using
the Maxwell SEV 16 cell kit (Promega, USA) with the
following pretreatment: After incubation, the mycelium
was collected by centrifugation at 3000 g for 10 min;
DNA was extracted from the fungal pellet by vortexing
for 30 min with 0.5 mm microbeads (Omni international,
USA), followed by a chemical lysis with 20 ll proteinase
K in 200 ll ATL buffer and 180 ll AL buffer (all three
manufactured by Qiagen, Germany). Following this
pretreatment, DNA was extracted with the MaxwellÒ
(Promega, USA) equipment following the manufac-
turer’s instructions. At UZ Leuven, DNA was extracted
using the Molzym DNA extraction kit (Molzym,
Germany), as recommended by the manufacturer.
In both NRCs, the ITS2 region was amplified using the
ITS86 forward primer 50 -GTGAATCATCGAATCTTT-
GAAC-30 and the ITS4 reverse primer 50 -
TCCTCCGCTTATTGATATGC-30 [10]. The ITS1
region was also amplified at UZ Leuven, using the
GeneAmp 9700 Proflex platform (Applied Biosystems),
with the ITS1 forward primer 50 -TCCGTAGGT-
GAACCTGCGG-30 and the ITS4 reverse primer. Purifi-
cation of PCR products was then performed using the
Exosap IT technique (Amersham, GE Healthcare Europe
GmbH, Belgium) at CHU Liège, while the Qiagen PCR
purification kit (Qiagen, Germany) was used at UZ
Leuven. Cycle sequencing was done on a classical
thermocycler (Thermohybaid, ThermoScientific, Bel-
gium). Bidirectional sequence data were generated after
purification using the BigDye terminator sequencing kit
(Applied Biosystems, Life technologies, Belgium).
Amplified products were finally purified using the clean
Seq Agencourt kit (Beckman Coulter Life Science,
France) or using spin columns followed by dissolving in
formamide at UZ Leuven. Sequencing was done on the
automate ABI 3500/3500XL (Applied Biosystems, Life
Mycopathologia (2021) 186:399–409
technologies, Belgium) at CHU Liège, while on
ABI3730xl at UZ Leuven. Sequences were edited using
the ABI Sequence Scanner V.1.0 software (Applied
Biosystems, Life technologies, Belgium) at CHU Liège,
while using the CLC Main Workbench 7.7.3 software
package (Qiagen) at UZ Leuven. Sequences generated by
the software were then compared to the CBS database,
which comprises several databases including Genbank
(http://www.cbs.knaw.nl).
For this survey, the three species T. mentagro-
phytes, T. benhamiae and T. interdigitale were gath-
ered under the name of T. mentagrophytes complex
because both laboratories (UZ Leuven and CHU
Liege) were not distinguishing the three species.
However, it should be mentioned that T. interdigitale
is theoretically the only one implicated in onychomy-
coses, but for harmonization, the appellation T.
mentagrophytes complex was kept in this manuscript.
Statistical Analysis
Statistical analysis was performed using the SAS
software (version 9.4) and a logistic regression test has
been applied. Results were considered statistically
significant when p value was \ 0.05.
Results
During the 2012–2016 period, 14,271 samples with a
positive fungal culture were treated by the two NRCs.
A total of 2733 samples were identified in 2012, 3185
Fig. 1 Global distribution of dermatophytes in Belgium between 2012 and 2016 (from all specimen types)
401
in 2013, 3264 in 2014, 2563 in 2015 and 2526 in 2016.
Among these positive samples, yeasts were identified
from 16% of the samples, and non-dermatophyte
molds from 42% of the samples. A total of 741
samples were identified as dermatophytes in 2012,
1516 in 2013, 1279 in 2014, 1249 in 2015 and 1384 in
2016.
Overall, considering all sampling sites, T. rubrum
was the predominant species (see Fig. 1 and Table 1
for distribution), with a significant increase in its
frequency from 45.8% in 2012 to 69.4% in 2016
(p \ 0.0001). Conversely, the frequency of the T.
mentagrophytes complex decreased significantly from
31.9% to 15% over the same period (p \ 0.0001). The
frequency of the other species remained quite
stable during the study period, with slight and no
significant variations depending on the year and
origins considered (p [ 0.05).
Dermatophytes Causing Tinea capitis
Figure 2 shows the frequency of dermatophytes
causing Tinea capitis. Microsporum audouinii was
the major pathogen during the study period. Indeed,
prevalence of this anthropophilic species decreased
from 56.4% in 2012 to 31.9% in 2014 but reached
again 66.5% in 2016. Statistical analysis showed for
this species a tendency to increase during the study
period (p = 0.06). Trichophyton tonsurans remained
quite stable, representing from 6.1 to 10.4% of the
isolates during the 5-year period. The zoophilic
species M. canis was the causative agent of 14.9% of
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Table 1 Dermatophyte species identified during the period 2012–2016 (number of isolates, and percentage)
2012 2013 2014 2015 2016

A. phaseoliforme 0 1 (0.07%) 0
A. quadrifidum 0 1 (0.06%) 0 0 1 (0.07%)
E. floccosum 0 5 (0.3%) 1 3 (0.24%) 2 (0.14%)
M. canis 44 (5.95%) 68 (4.48%) 117 (9.17%) 61 (4.88%) 29 (2.09%)
M. ferrugineum 0 0 2 (0.15%) 0 0
M. audouinii 71 (9.58%) 177 (11.68%) 43 (3.36%) 85 (6.9%) 117 (8.46%)
N. gypsea 0 3 (0.19%) 4 (0.31%) 0 0
N. persicolor 0 1 (0.06%) 6 (0.46%) 0 0
N. praecox 2 (0.27%) 0 3 (0.23%) 0 0
P. cookei 0 0 0 1 (0.08%) 0
T. mentagrophytes complex 236 (31.9%) 296 (19.5%) 170 (13.3%) 197 (15.8%) 207 (14.97%)
T. rubrum 339 (45.87%) 808 (53.47%) 842 (66.22%) 841 (67.6%) 963 (69.9%)
T. schoenleinii 0 5 (0.3%) 0 0 0
T. soudanense 5 (0.67%) 47 (3.1%) 22 (1.72%) 34 (2.75%) 25 (1.8%)
T. verrucosum 0 1 (0.06%) 1 (0.07%) 2 (0.16%) 2 (0.14%)
T.tonsurans 18 (2.4%) 39 (2.57%) 40 (3.13%) 15 (1,2%) 27 (1.96%)
T. violaceum 26 (3.5%) 65 (4.28%) 27 (2.1%) 10 (0.8%) 9 (0.065%)
Trichophyton sp. 0 0 0 0 2 (0.14%)

Fig. 2 Dermatophyte distribution in hair samples collected in CHU Liège/UZ Leuven during the study period

TC cases in 2015, while its prevalence decreased to
5.2% in 2016. African species such as T. violaceum
and T. soudanense were also present in Belgium, with
T. violaceum being more prevalent in 2012 and 2013
compared to 2016 (decrease from 18.1% in 2012 to
2.3% in 2016, p \ 0.0001). On the contrary, the
frequency of T. soudanense markedly increased,
reaching 12.1% of all TC cases in 2016 against 1.1%
in 2012 (p \ 0.016). Species of the T. mentagrophytes
complex were also represented in the Belgian study
cohort (3.2%–1.7% between 2012 and 2016). As TC
affects essentially children, the species distribution in

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Mycopathologia (2021) 186:399–409 403

Fig. 3 Dermatophyte distribution (number of cases) in hair samples during the study period in children younger than 10 years

patients younger than 10 years is shown in Fig. 3.
Microsporum audouinii was the main causative agent
of TC in children, representing more than half of the
cases (57.8%), followed by T. violaceum (12.8%), T.
soudanense (11.4%), M. canis (7.7%) and T. tonsurans
(7.6%). Trichophyton rubrum and species of the T.
mentagrophytes complex were rarely represented in
this age group, representing 0.4% and 1.9% of the
cases, respectively.
Dermatophytes Implicated in Skin Infections
Dermatophytosis of the glabrous skin was essentially
caused by T. rubrum. The frequency of T. rubrum in
skin infections increased from 34.9% in 2012 to 61.4%
in 2016 (p \ 0.0001). Species of the Trichophyton
mentagrophytes complex were also well represented
in the studied population, however, their frequency
decreased from 38% in 2012 to 20.5% in 2016
(p \ 0.0001). Microsporum audouinii was less often
represented in skin samples; it was mainly causing TC

Fig. 4 Dermatophyte distribution in skin samples during the study period

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in Belgium, and only sporadically dermatophytosis of
the glabrous skin (decreasing from 5.2 to 0.8% over
the study period). Other species such as M. canis and
T. tonsurans were also detected in skin samples from
several body parts, but to a lesser extent. The
distribution of dermatophytes responsible for skin
infections is shown in Fig. 4.
Dermatophytes Causing Onychomycosis
Trichophyton rubrum was clearly the major agent of
onychomycosis. Since 2012 its isolation rate increased
from 59.8% to 83.8% (p \ 0.0001). Conversely, the
frequency of species of the T. mentagrophytes com-
plex in onychomycosis was decreasing, ranging from
35.2% in 2012 to 15.9% in 2016 (p \ 0.0001). Other
species were involved in onychomycosis, but to a
lesser extent, such as M. canis, T. tonsurans, T.
schoenleinii, T. soudanense, T. violaceum, E. flocco-
sum, N. gypsea, N. persicolor, M. ferrugineum and N.
praecox. In Fig. 5, only T. rubrum and the T.
mentagrophytes species complex are represented.
The other species less implicated (less than 1% each)
are not shown on this graph.
Rare Dermatophytes Species Isolated During
the Study Period
During the period 2012–2016, less common dermato-
phytes (less than 1% considering all sampling sites)
were isolated by the NRCs such as N. persicolor, M.
Fig. 5 Dermatophyte distribution in nail samples during the study period
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Mycopathologia (2021) 186:399–409
ferrugineum, A. quadrifidum, E. floccosum, P. cookei,
N. praecox, T. schoenleinii and A. phaseoliforme
which were recovered from some nails, hair or skin
samples.
Dermatophytes Distribution by Age
Prevalence of dermatophytes infections increased with
age in the studied population, the maximum being
observed within the population older than 50 years
with 2105 infections caused by dermatophytes
between 2012 and 2016 (see Fig. 6). Regarding the
most prevalent dermatophyte species, 1000 cases
concerned patients younger than 10 years, most of
them being cases of Tinea capitis (65.2% of the cases)
which were caused essentially by M. audouinii.
Indeed, among this age group, M. audouinii was
responsible for 42% of the infections (n = 420),
followed by M. canis (n = 108, 10.8%), T. rubrum
(n = 108, 10.8%), T. violaceum (n = 102, 10.2%), T.
soudanense (n = 95, 9.5%), T. tonsurans (n = 87,
8.7%) and the T. mentagrophytes species complex
(n = 80, 8%). Ninety-two cases of onychomycosis due
to T. rubrum were also observed in this population
during the study period. For older people, T. rubrum
and T. mentagrophytes complex were the major
etiological agents of dermatomycoses. In patients
older than 50 years, T. rubrum was predominant,
accounting for 68.5% of the total number of infections
(See Table 2).
Mycopathologia (2021) 186:399–409 405

Fig. 6 Distribution of dermatophyte infections according to the age during the study period

Dermatophytes Following Gender followed by species of the T. mentagrophytes com-

Gender was not recorded for all cases included in the
study as this information often is not given on the NRC
form associated with the sample. For cases for which
the variable gender was registered (n = 6114), the
male to female ratio was 1.3 for dermatophyte
infections, stressing that males were more often
infected than females (respectively, 3438 vs. 2676
cases, p \ 0.0001).
Discussion
This study covering the 5-year period 2012–2016
shows that T. rubrum was still the main agent
responsible for dermatophytosis in Belgium. This
dermatophyte was essentially detected in nail and skin
samples where it was the dominant species identified,
plex. Considering onychomycosis, its incidence was
even increasing, in contrast to species of the T.
mentagrophytes complex. This is not surprising as T.
rubrum is the main etiological agent of onychomyco-
sis in many countries all around the world including
Europe [11–16], North and South America [17–20],
Africa [21], India [22] and Korea [23, 24].
For example, in a similar retrospective study
covering the period 2005–2009 in Sweden, Trichophy-
ton rubrum was the predominant pathogen isolated
from nails with a prevalence of 83.2%, followed by T.
mentagrophytes (7.4%) [11]. Likewise, T. rubrum was
the main species (37%) isolated from nails in a tertiary
care hospital in Italy during the period 2004–2006
[15]. In Eastern Europe, T. rubrum was the most
frequent species identified in fingernail dermatophyte
onychomycosis (90.9%), toenail onychomycosis
(77.7%) and Tinea pedis (65.6%) during an earlier

Table 2 Distribution of dermatophyte species according to the age

Age M. M. canis T. mentagrophytes T. rubrum T. T. T.
audouinii complex tonsurans soudanense violaceum

\ 10 years 420 (88.4%) 108 80 (6.8%) 108 (3%) 87 (65.9%) 95 (78%) 102 (80.3%)
(56.3%)
11–30 years 29 (6.1%) 44 (22.9%) 159 (13.4%) 768 (21.4%) 21 (15.9%) 11 (9%) 16 (12.6%)
31–50 years 18 (3.8%) 20 (10.4%) 327 (27.7%) 1281 14 (10.6%) 8 (6.5%) 3 (2.4%)
(35.6%)
[ 50 years 8 (1.7%) 23 (12%) 615 (52.1%) 1435 (40%) 10 (7.6%) 8 (6.5%) 6 (4.7%)
All 475 192 1181 3592 132 122 127

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period 1995–2002 [25]. In Mexico, T. rubrum was
again the predominant dermatophyte species during
the period 1996–2005 [20]. As observed in our study,
the annual incidence of patients with T. rubrum
infections had been increasing in Korea during the
period 1979–2013, and of 131.122 patients with
dermatophytosis, 115.846 patients (88.35%) had a T.
rubrum infection [23]. This team also noticed a
decrease in the frequency of T. mentagrophytes during
the period 1992–2012 [24].
Trichophyton rubrum was also the most frequent
species isolated from skin infections in Belgium
(essentially from Tinea pedis), followed by mem-
bers of the Trichophyton mentagrophytes complex
as it is the case in many industrialized countries
worldwide [2]. A few M. canis isolates were
recovered from skin infections in Belgium. In some
countries such as Slovenia, M. canis was more
prevalent than T. rubrum in skin infections [25]. In
Germany, it was the second more common
zoophilic agent responsible for skin infection, T.
benhamiae ranking the first [26]. In our study, the
dermatophytes distribution in skin samples was
quite similar to that described in New Zealand
during the period 1999–2002 where T. rubrum was
the more prevalent, followed by T. mentagrophytes
and M. canis [27]. Few T. verrucosum isolates have
been isolated in Belgium, probably due to the
decrease in rural areas in our country. Epidermo-
phyton floccosum was also rarely diagnosed in our
country, in comparison with other countries such as
Iran, where this species is the first etiological agent
responsible for skin dermatophytosis [28].
In 2014, we noticed an increased number of
infections of the skin and the scalp due to T.
benhamiae. This species has been reported for the
first time in Japan in 2001 [29]. We clearly do not
know if this species arrived only in 2014 in Belgium or
if its previous absence was due to misidentification
with M. canis or T. interdigitale. Until 2016, T.
benhamiae was included in the T. mentagrophytes
complex, which explains why it was not distinguished
from this complex in our study. Since now and
following the phylogenetical classification of the
Hoog et al. [3, 4], this species is differentiated from
T. interdigitale.
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Mycopathologia (2021) 186:399–409
Regarding Tinea capitis, as it has been shown for
several other countries, we noticed an increasing
etiological role of anthropophilic species [30]. The
main species responsible for Tinea capitis in Belgium
is the African anthropophilic fungus M. audouinii.
This dermatophyte is a common agent of scalp and
skin infections, being the most prevalent dermato-
phyte isolated from patients with Tinea capitis in
certain African countries [31–33] Its abundance in
Belgium is probably due to immigrations waves from
Central Africa such as Cameroon and Democratic
Republic of Congo. Indeed, a lot of migrants incoming
in Belgium are from this part of Africa [34]. This
dermatophyte has been responsible for large scholar
outbreaks but it has been eradicated in Europe after the
massive use of griseofulvin. In western Europe, M.
audouinii is still present in Switzerland where it has
been responsible for school outbreaks [35]. In a study
of M. audouinii dermatophytosis in Germany, authors
reported that this species was introduced to the city by
children coming from vacations in Africa and then
spread to other children in communities and among
members of their families [36]. A recent work done in
the urban area of Paris during five years on Tinea
capitis showed that M. audouinii is well represented in
France as 28.2% of TC cases were caused by this
dermatophyte. However, T. soudanense and T. ton-
surans were more prevalent, causing 38.3% and
33.5% of TC cases, respectively, during the study
period. In this study, authors pointed an important
increase in the frequency of T. tonsurans. Such an
increase was not seen in our study. On the contrary, a
decrease in the frequency of T. soudanense and M.
audouinii was observed in France, while their fre-
quency globally increased in our study [37, 38]. This
observation should be explained by different immi-
gration profiles between the two countries. However,
what is surprising is that in Paris, T. tonsurans
continuously increased, mostly in patients from West
Africa who are generally infected by the anthro-
pophilic M. audouinii and T. soudanense. The pre-
dominance of T. tonsurans was also seen in Caribbean
patients, more precisely from Haiti where T. tonsurans
is the major species giving rise to TC. This latter
observation should explain the lower incidence of T.
tonsurans in Belgium, where immigration from Car-
ribean countries is not so frequent than in France.
A recent review of the literature showed that M.
audouinii is still present in every continent, as cases
Mycopathologia (2021) 186:399–409
have been reported in Australia, Jamaica, Nepal,
Mexico, Malaysia, Dominican Republic and many
countries of North and South Europe [39]. In 2016, a
major part of TC cases was caused by M. audouinii
and six genotypic variants of this species were
circulating in Belgium [34]. Surprisingly, this species
is poorly represented in other European countries. This
fact has been reviewed by Zhan et al. [16], who
reported M. canis, T. violaceum and T. tonsurans as
the main etiological agents of TC in Europe but also
worldwide. In Denmark, M. canis is responsible for
most cases of TC, and M. audouinii was rarely isolated
from 1993 to 2003 [40]. In the same study, an increase
was also noticed in the frequency of the anthropophilic
T. violaceum in Tinea capitis, but not for M. audouinii.
There is probably immigration in this country, but no
importation of M. audouinii at the time of the study
which is older than ours. Similar observation was
reported in Eastern Europe such as Slovenia and
Poland, with M. canis being the most frequent
dermatophyte isolated from Tinea capitis and no or
few M. audouinii isolates. Conversely, an increase in
the number of T. tonsurans isolates only was seen in
Poland, which may be caused by the increasing
migration of population in the recent years, after
Poland had entered European Union [25, 30, 41, 42].
These discrepant results may be related to differences
in the African countries from which the migration
comes. Another explanation for the high frequency of
M. audouinii in Belgium could be the use of
terbinafine as treatment of choice for this agent.
Indeed in other countries such as France, griseofulvin
is used for treatment of Tinea capitis. One may
speculate a lower susceptibility of M. audouinii to
terbinafine, requiring longer treatment duration, and a
greater risk for transmission related to longer time
until resolution of the infection. A meta-analysis of
randomized clinical trials comparing the efficacies of
oral terbinafine and oral griseofulvin for the treatment
of childhood Tinea capitis has shown that while there
was no clear difference in the activity between
terbinafine and griseofulvin for Trichophyton species,
terbinafine was less efficient on Microsporum species
than griseofulvin [43]. Another reason for the few
reports of M. audouinii in other countries could be the
lack of molecular tools such as ITS PCR which may
lead to misidentification. The lack of sensitivity of
phenotypic tools including culture and direct exami-
nation is a real problem and can largely contribute to
407
misidentification or lack of identification of M.
audouinii.
Regarding Tinea capitis in children the last study
reported in Belgium was published by Kolivras et al.
[6] in 2002, where they followed 122 children from the
St Pierre Hospital Brussels. The implicated anthro-
pophilic dermatophytes were by decreasing fre-
quency: M. audouinii (39.34%), T. soudanense
(28.69%), T. violaceum (18.03%) and T. tonsurans
(3.28%). These data are not so different from the
present study realized more than 10 years after.
Microsporum audouinii (57.8% of the cases) was the
main etiological agent detected, followed by T.
violaceum (12.8%), T. soudanense (11.4%), M. canis
(7.7%) and T. tonsurans (7.6%). However in the
present survey, M. audouinii and T. tonsurans were
more prevalent compared to the study of Kolivras et al.
[6], while T. soudanense and T. violaceum decreased.
In children lower than ten, 92 cases of onychomy-
coses due to T. rubrum were diagnosed between 2012
and 2016. This is not surprising as onychomycoses can
also affect young children. The reported prevalences
of onychomycosis in children range from 0.2 to 2.6%
[44–49]. Several cases have already been described,
for example, in Denmark where a case of onychomy-
coses due to T. rubrum was diagnosed in a 2-year-old
baby [50]. Between 2008 and 2009 in Berlin,
Germany, 24 children were diagnosed with ony-
chomycoses due to T. rubrum [49]. Likewise, records
from a decade of dermatological consultations have
been analyzed in Poland. Ninety-nine cases of ony-
chomycosis were diagnosed in the 0–18 years old
population, representing 19.8% of all confirmed cases
of superficial mycosis (500 cases). Fingernail ony-
chomycosis was recognized in 52 (10.4%) cases;
children under 3 years of age were predominantly
involved. Toenail onychomycosis concerned 47
(9.4%) patients, and its incidence increased steadily
with increasing age. Trichophyton rubrum was the
most common etiological agent [47]. Onychomycoses
in children 0–18 were also diagnosed in Korea,
representing 2.3% of all onychomycoses [51], and T.
rubrum was the most common etiological agent also
(51.3%).
The prevalence of dermatomycosis was also found
to be higher in men than women, as reported by other
authors all around the world [52–54], possibly because
men do not take care of their nails as women.
123
408
Conclusion
The findings presented here are in agreement with
previous studies showing T. rubrum as the predomi-
nant dermatophyte species in the general population of
industrialized countries in Europe. The rise of infec-
tions by T. rubrum is probably due to the improvement
of sanitary conditions, the increase in traveling,
practice of sports, use of occlusive footwear and the
use of public facilities such as communal showers and
swimming pools. Nevertheless, an increasing preva-
lence of anthropophilic species such as M. audouinii,
T. soudanense and T. violaceum was also observed in
cases of Tinea capitis, probably due to immigration
waves from African countries.
Author contributions All authors contributed to the study
conception and design. Material preparation, data collection and
analysis were performed by RS, AA and RD. The first draft of
the manuscript was written by RS, KL, LC and MPH
commented and contributed on previous versions of the
manuscript. MPH supervised and validated the study. All
authors read and approved the final manuscript.
Funding None.
Declaration
Conflicts of interest Authors declare no conflicts of interest.
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