DOI: 10.1111/pde.

13446

Pediatric
ORIGINAL ARTICLE Dermatology

Emergence of African species of dermatophytes in tinea

capitis: A 17-year experience in a Montreal pediatric hospital

Danielle Marcoux MD1 | Julie Dang MD2 | Hedwige Auguste MD, MSc3 |
Catherine McCuaig MD1 | Julie Powell MD1 | Afshin Hatami MD1 |
Catherine Maari MD1 | Jean-Baptiste Le Meur MSc4

1
Division of Pediatric Dermatology,
Department of Pediatrics, Sainte-Justine Abstract
University Hospital Center, Montreal, QC, Background/Objectives: An increase in dermatophyte infections caused by African
Canada
2 species is reported in countries receiving African immigrants. Our goal was to deter-
Faculty of Medicine, University of
Montreal, Montreal, QC, Canada mine the epidemiologic and clinical characteristics of tinea capitis in children
3
Public Health, University of Montreal, infected with African species of dermatophytes in Montreal, Canada.
Montreal, QC, Canada
4
Methods: Demographic and clinical data from medical records of children infected
Department of Social and Preventive
Medicine, Faculty of Medicine, Laval with African species of dermatophytes were retrieved retrospectively (2000-2016)
University, Quebec, QC, Canada
at Sainte-Justine University Hospital Center.
Correspondence Results: In Montreal, the number of tinea capitis cases caused by African species of
Danielle Marcoux, MD, Division of
dermatophytes increased sixfold over 17 years. African immigrant children (84%),
Dermatology, Sainte-Justine University
Hospital Center, Montreal, QC, Canada. men and boys (61%), and preschoolers (2-5 years old) (51%) were the most fre-
Email: danmarcoux@videotron.ca
quently affected in our 315 cases. Family contamination was frequent (45%). Refer-
Funding information ring physicians prescribed systemic antifungal treatment in 39% of cases and
University of Montreal Faculty of Medicine
pediatric dermatologist consultants in 90%. Treatment failure to oral terbinafine
summer research scholarship (Comite
d’Organisation du Programme des Stages occurred in 39% of Microsporum audouinii infections.
e
d’Et ) (2616).
Conclusion: In Montreal, there was a significant increase in tinea capitis caused by
African species of dermatophytes. Microsporum audouinii is highly transmissible and
often resistant to oral terbinafine. Recognizing tinea capitis trends in a given envi-
ronment will improve patient care.

KEYWORDS
fungal, hair disorders, infection

1 | INTRODUCTION prevalence ranging up to 15%, mostly in African-American children.3

Trichophyton or Microsporum species almost exclusively cause tinea
capitis (TC), a zoophilic, anthropophilic, or geophilic dermatophyte
scalp infection frequent in prepubertal children.1,2 In Western Eur-
ope and North America, in the 19th and early 20th century, the
most common species was anthropophilic Microsporum audouinii.2
Later, in Europe, zoophilic M. canis affected mainly Caucasian chil-
dren.2 In North America, from the 1950s on, anthropophilic Tri-
chophyton tonsurans became the dominant cause of TC,1 with a
M. audouinii, T. violaceum, and T. soudanense are predominant in
many parts of Africa.4
Sainte-Justine University Hospital Center (SJUHC) serves a large
multicultural population in the Montreal area, including an increasing
number of African immigrants.5,6 This study aimed to identify epi-
demiologic changes and clinical characteristics of children with TC
due to African species of dermatophytes, as well as how referring
physicians and pediatric dermatologist consultants managed TC to
improve their diagnosis and treatment.

Pediatric Dermatology. 2018;1–6. wileyonlinelibrary.com/journal/pde © 2018 Wiley Periodicals, Inc. | 1

2 | Pediatric
Dermatology
2 | METHODS
The SJUHC Institutional Review Board approved the study. What-
ever the severity of the clinical presentation, the hospital physician
suspected TC, the patient had a scalp and hair calcofluor direct
examination, and a fungal culture was taken. A retrospective data-
base analysis was performed on the medical records of all SJUHC
patients with positive mycologic cultures for M. audouinii, T. souda-
nense, T. violaceum, and T. schoenleinii from 2000 to 2016.
Demographic and clinical data were retrieved from patient
records. African immigrant children were defined as first- or second-
generation immigrants from Africa. Diagnosis by referring physicians
(pediatricians, family physicians, community dermatologists) and
SJUHC pediatric dermatologist consultants on the initial visit to our
center and treatment prescribed were recorded. Diagnoses retrieved
from medical charts were categorized as definite TC (TC stated by
the physician as definite diagnosis), possible TC (TC stated by the
physician as a possible diagnosis), and “other” diagnosis. Treatment
options were categorized into six groups: oral antifungals, topical
antifungals, corticosteroids, antibiotics, other, and none.
Data were analyzed using descriptive statistics (means, medians,
percentages) to portray the affected population, clinical presentation
of TC, prescribed treatment, and evolution of lesions. Trends in
annual proportions of TC cases due to African dermatophyte species
were tested using the chi-square test. Diagnostic accuracy and treat-
ment adequacy of referring physicians and pediatric dermatologist
consultants were assessed according to percentage of concordance.
FIGURE 1 Proportion of all tinea capitis-positive cultures due to African dermatophyte species over 17 y
MARCOUX ET AL.
Statistical analyses were conducted using R 2.12.1 (R Foundation for
Statistical Computing, Vienna, Austria).
3 | RESULTS
3.1 | Number of TC cases
A total of 1378 hair and scalp fungal cultures were positive for der-
matophytes at the SJUHC mycology laboratory from 2000 to 2016.
The overall number of positive fungal cultures for TC remained rela-
tively stable (56-97 cases per year, average 81 cases per year) with no
statistically significant linear trend over the entire period (P = .17). Dur-
ing that period, T. tonsurans was isolated in 942 (68%) cases and
M. canis in 95 (7%). Trichophyton rubrum (n = 16), T. verrucosum (n = 5),
M. gypseum (n = 3), and T. mentagrophytes (n = 2) accounted for a
combined total of 1.9%. African dermatophyte species (M. audouinii,
T. soudanense, T. violaceum, T. schoenleinii) were identified in 315 (23%)
cases. By the end of 2016, African dermatophyte TC infections had
increased sixfold (from 6 cases in 2000—7% of TC positive cultures—
to 37 in 2016—39% of TC positive cultures, P < .001), and their overall
distribution was 148 (47%) M. audouinii, 121 (38%) T. soudanense, 45
(14%) T. violaceum, and 1 (0.3%) T. schoenleinii (Figure 1).
3.2 | Demographic characteristics
Five children had two separate infectious episodes, for a total of
310 patients and 315 cases of TC due to African dermatophyte
MARCOUX ET AL.
species. Boys were more frequently infected (61%). Twenty-five chil-
dren were infected when they were younger than 2 years old, 161
at 2-5 years old, 120 at 6-11 years old, and 9 at 12-18 years old
(Figure 2). Mean age at infection was 5.7  3.0.
Family geographic origin was known for 257 of 310 children
(83%); 215 (84%) were first- or second-generation emigrants from
Africa, who were born in Africa (58%), Canada (32%), or other
countries (10%).
Pediatric | 3
Dermatology
In 142 of 315 cases (45%), one or more family household mem-
bers had TC, with or without tinea corporis or faciei, due to the
same dermatophyte species as the proband; 3% were in contact with
infected individuals at daycare, school, or extended family.
Failing systemic therapy was defined as having a positive culture
or clinical evaluation of the scalp after 6-8 weeks of oral antifungal
treatment. More terbinafine therapy failure was observed than of
griseofulvin therapy failure, particularly in M. audouinii infections.

3.3 | Clinical features and contamination source
Information on clinical features, duration of infection before SJUHC
initial visit, and treatment response is presented in Table 1.
Dermatophyte infection duration before SJUHC initial visit was
documented for 243 patients: it had been present from less than 2
weeks to over 1 year. with a median time interval of 2-6 months.
3.4 | Diagnostic accuracy and treatment adequacy
Of the 226 cases that referring physicians and pediatric dermatolo-
gist consultants saw, referring physicians diagnosed definite TC in
184 (81%) and pediatric dermatologist consultants diagnosed definite
TC in 211 (93%), indicating a concordance for diagnosis of 84%.
Referring physicians prescribed oral antifungals in 89 (39%) cases

F I G U R E 2 Distribution of African
dermatophyte species according to age
(N = 315)

T A B L E 1 Clinical features of tinea capitis due to African dermatophyte species

Microsporum audouinii, T. soudanense, T. violaceum, T. schoenleinii, Total,
n = 148 n = 121 n = 45 n=1 N = 315

Clinical presentation n/N (%)

Scaly patches with alopecia 93 (63) 63 (52) 22 (49) 1 179
Scaly patches without alopecia 47 (32) 45 (37) 14 (31) 106
Kerion 8 (5) 13 (11) 9 (20) 30
Duration of infection, mo
<2 52 (35) 33 (27) 15 (33) 1
2-6 33 (22) 31 (25) 13 (29)
6-12 10 (7) 8 (7) 0 (0)
> 12 18 (12) 19 (16) 11 (25)
Missing 35 (24) 30 (25) 6 (13)
Treatment failure with oral terbinafine 55/141 (39) 6/117 (5) 1/40 (3) 0
Treatment failure with oral griseofulvin 4/76 (5) 1/20 (5) 0/15 (0) 0

T, Trichophyton.
4 | Pediatric MARCOUX ET AL.

Dermatology
and pediatric dermatologist consultants in 204 (90%). The concor-
dance for adequate treatment with oral antifungals prescribed by
referring physicians and pediatric dermatologists was 46%.
and makes hair loss and scaling of the scalp more noticeable, facili-
tating TC recognition in boys.5 Similarly to the literature,1,17,19
preschoolers (2-5 years old) were most frequently affected (51%).
Children under 23 months of age accounted for 8% (Figure 2).

4 | DISCUSSION
4.1 | Number of TC cases
In recent decades, an increase in TC due to African species of der-
matophytes has been reported from cosmopolitan centers in Europe
and the Middle East (Table 2).7-18 In the Montreal area over the past
17 years, although the overall number of TC cases did not change
significantly (mean 344 per year), there was a sixfold increase in
African species of dermatophyte infections in children mainly due to
anthropophilic M. audouinii and T. soudanense (from 6/82 [7%] in
2000 to 37/95 [39%] in 2016). Conversely, the rate of cases of
T. tonsurans dropped from 67 out of 82 (82%) in 2000 to 41 out of
95 (43%) in 2016. Increased immigration to the Montreal area from
countries endemic for M. audouinii, T. soudanense, and T. violaceum
and international travel could explain these changes. Montreal has
the third largest immigrant population in Canada, growing 36% from
2001 to 2011.5 In 2006, immigrants settling in Montreal originating
6
from Africa accounted for 29% of the immigrant population.
4.2 | Demographic characteristics
In our cohort, more than 84% of TC due to African species of der-
matophytes were identified in first- or second-generation immigrants
from Africa, mainly boys. Although boys and girls have similar con-
tamination risk factors related to fomites, such as clippers for boys
or brushes, combs, and hair ornaments for girls,19 one hypothesis is
that shorter hair facilitates scalp contact with infectious spores17
4.3 | Clinical features and contamination source
Twenty percent of T. violaceum infections developed kerions, as
opposed to 11% for T. soudanense and 5% for M. audouinii infections,
consistent with reports indicating that M. audouinii infections are usu-
ally noninflammatory, unlike T. violaceum infections.4 Delay in diagno-
sis (2-6 months) increases the risk of transmission to household
members with anthropophilic species, especially in poor socioeco-
nomic and crowded living conditions.19 Family members developed TC
or tinea corporis or faciei due to the same agent in 45% of our cases,
and 3% of our cases acquired the infection at daycare or school or
through members of the extended family. Asymptomatic carriers are a
major contamination source. All family household members with
lesions should be screened and treated accordingly.
Hair care and grooming practices should also be investigated
because certain hair grooming practices favored higher rates of
transmission (nonsterilized razors and clippers,14 male cropped hair-
styles, female tight hair plaiting). Genetic susceptibility and limited
access to health care may also play a role.18 Tools used in hairdress-
ing salons have been shown to be reservoirs of anthropophilic der-
matophytes.14
4.4 | Diagnostic accuracy and treatment adequacy
There was acceptable concordance for the diagnosis of definite TC
between referring physicians (81%) and pediatric dermatologist con-
sultants (93%). Topical therapy, such as antifungal shampoos,

T A B L E 2 Epidemiology of tinea capitis between 1998 and 2016 with the three dermatophyte species most frequently isolated
1 2 3

Country (city or area) Y Cases, n Species (%) Author

Belgium 2012-14 498 M. audouinii (36) T. violaceum (13) M. canis (7.2) Sacheli7
France (Paris) 2010-15 1311 T. soudanense 38.3) T. tonsurans (33.5) M. audouinii (28.2) Gits-Muselli8
Ireland 2004-05 62 T. tonsurans (75.8) M. ferrugineum (12.9) Hackett9
Israel (Tel Aviv) 2010-14 145 T. violaceum (44.8) M. audouinii (40) Mashiah10
Israel 2012-13 90 T. violaceum (47.7) M. canis (45.5) Shemer11
Italy (Milan) 2004-11 86 T. violaceum (38.3) Mapelli12
Italy (Northern) 2005-13 53 T. violaceum (43) T. soudanense (56) Farina13
Mali 2009 590 T. soudanense M. audouinii Coulibaly14
Portugal (Lisbon) 2004-13 236 M. audouinii (51) T. soudanense (19) Verissimo15
Spain (Coruna) 2009-14 16 M. canis (80) T. violaceum (13) valo Bermudez16
Are
Switzerland (Zurich) 2006-13 90 T. violaceum (36.7) M. audouinii (23.3) Kieliger17
United States (Northern 1998-2007 6,723,730 T. tonsurans (91.8) M. audouinii (3) Mirmirani18
California, Kaiser Permanente)
Canada (Montreal) 2000-16 1,378 T. tonsurans (68.4) M. audouinii (11) T. soudanense (9) Marcoux
Canada (Montreal) 2016 95 T. tonsurans (43) African species (38.9) M. canis (12.6) Marcoux

M, Microsporum; T, Trichophyton.
MARCOUX ET AL.
although not adequate for treating active TC, may reduce the rate of
carriage and risk of transmission to others,20 but referring physicians
were much less likely to initiate adequate systemic antifungal treat-
ment (89/226, 39%) than pediatric dermatologist consultants (204/
226, 90%).This acceptable diagnosis and poor treatment concor-
dance between referring physicians and pediatric dermatologist con-
sultants suggests a gap in the recognition of adequate treatment of
TC or preferred patient referral for systemic treatment to pediatric
dermatologists. Furthermore, resistance to terbinafine of M. audouinii
infections is frequently encountered and underestimated.
4.5 | Prescription patterns
Griseofulvin remains the TC treatment of choice in the United
States, France, and United Kingdom and has a high cure rate for
20-22
T. tonsurans and T. violaceum infections. Terbinafine demon-
strated potent antifungal activity against various dermatophyte spe-
cies, although it is much more efficacious against Trichophyton than
Microsporum infections.23 Prescriptions for antifungal drugs such as
terbinafine, itraconazole, and fluconazole have increased because
of their shorter and simpler treatment regimens and accessibil-
18,23
ity. In a group of Israeli children, griseofulvin and fluconazole
were shown to reduce potential disease transmission and eradicate
TC, although griseofulvin was more effective than fluconazole
against M. canis infections.11 At our center, TC cases were treated
for at least 6 weeks with terbinafine 62.5 mg/d for children weigh-
ing less than 20 kg, 125 mg/d for those weighing 20-40 kg, and
250 mg/d for those weighing 40 kg. For Microsporum species
infections, griseofulvin 15-20 mg/kg per day was prescribed for at
least 6 weeks, but effective treatment often requires higher
dosages and longer treatment duration.22,23 From our experience,
we would recommend griseofulvin at a dose of 20-25 mg/kg for
8 weeks for Microsporum species infections. In Tunisia24 and
Egypt,25 a switch from T. violaceum to M. canis infections has been
observed. This further supports the importance of Wood’s lamp
examination and fungal culture before starting an antifungal agent
because we may encounter more Microsporum species infections in
the future.
We found a higher rate of treatment failures with terbinafine
(39%) than griseofulvin (5%) for M. audouinii infections. In our expe-
rience, terbinafine is not as effective as griseofulvin for clinical and
mycologic eradication of M. audouinii. This is consistent with other
studies reporting higher cure rates with griseofulvin than with newer
antifungals for Microsporum species.11,17,22,23 For terbinafine, we
suggest that dosing should be 6-8 mg/kg/d up to 250 mg/d for
Microsporum species infections. There are no recent data in the liter-
ature on the minimum inhibitory concentration of terbinafine for
Microsporum species, but it is possible that a higher minimum inhibi-
tory concentration or faster pharmacokinetics of terbinafine in chil-
dren could explain the observed treatment failures.
This retrospective study involves a limited number of cases with
short observation and follow-up periods from a single tertiary Mon-
treal pediatric hospital. Our data were collected from patients with
Pediatric | 5
Dermatology
positive fungal cultures and may not reflect actual TC prevalence in
our area. Nonetheless, our study provides important information on
the changes observed in the etiology of TC in the Montreal area.
5 | CONCLUSION
The rise in African anthropophilic dermatophyte species (M. au-
douinii, T. soudanense) infections could reflect increased immigration
from African countries and is a significant public health concern.
The high rate of household contamination suggests that all family
household members should be evaluated. Caretakers should initially
identify the country of origin and travel history. A Wood’s lamp
examination should be performed; infections due to M. audouinii
will produce a bright yellow-green fluorescence. M. audouinii’s resis-
tance to terbinafine and sensitivity to griseofulvin and other azole
agents should direct the physician to prescribe the latter for TC if
the Wood’s lamp examination is positive. Recognizing the emer-
gence of different dermatophyte species in a given environment
and their clinical features and antifungal sensitivity will improve
patient care.
ORCID
Julie Dang http://orcid.org/0000-0001-5624-2779
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How to cite this article: Marcoux D, Dang J, Auguste H,
et al. Emergence of African species of dermatophytes in tinea
capitis: A 17-year experience in a Montreal pediatric hospital.
Pediatr Dermatol. 2018;00:1–6. https://doi.org/10.1111/
pde.13446