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Epidemiology and Pathogenesis of Dermatophytes

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A special issue of Journal of Fungi (ISSN 2309-608X). This special issue belongs to the section "Fungal Pathogenesis and Disease Control".

Deadline for manuscript submissions: closed (15 October 2021) | Viewed by 32260

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Dr. Sophie Brun

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Laboratory of Parasitology-Mycology, Avicenne University Hospital, Bobigny, France
Interests: dermatophytes and dermatophytosis; biological diagnosis; epidemiology; resistance

Prof. Dr. Bernard R. Mignon

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Faculty of Veterinary Medicine, Fundamental and Applied Research for Animals and Health, University of Liège, Liège, Belgium
Interests: pathogenesis of dermatophytosis

Dr. Jean-Philippe Bouchara

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Univ Angers, Univ Brest, CHU Angers, IRF, SFR ICAT, F-49000 Angers, France
Interests: fungal respiratory infections; cystic fibrosis; epidemiology; biological diagnosis; pathogenic mechanisms; evasion to the oxidative stress; secondary metabolism
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Dear Colleagues,

Dermatophytes are filamentous fungi causing superficial infections of the skin and appendages in both humans and animals. These fungal infections represent a global health problem, attested by the number of people concerned and the huge consumption of antifungals worldwide. The pathogenesis and severity of dermatophytosis depend on various immunological and non-immunological factors such as the ecological origin (anthropophilic, zoophilic or telluric) of the dermatophyte involved, but also epidemiological and geographical factors, as well as some host genetic factors predisposed to susceptibility. Indeed, although they most often cause benign superficial infections, dermatophytes may sometimes be responsible for extensive or deep-seated infections that are difficult to treat. In addition, cases of resistance to antifungals, especially for Trichophyton spp., have been increasingly reported in recent years. Finally, molecular approaches have resulted in successive revisions of the taxonomy of these fungi and the description of novel genera and species, but molecular species definitions do not always coincide with existing concepts which are guided by ecological and clinical criteria, and the taxonomy of dermatophytes might be reconsidered.

This Special Issue will therefore focus on molecular epidemiology, pathogenesis (virulence factors of these fungi and the host response), polyphasic taxonomy and antifungal resistance mechanisms of dermatophytes, with a special emphasis on Trichophyton spp.

Dr. Sophie Brun
Prof. Bernard R. Mignon
Prof. Jean-Philippe Bouchara
Guest Editors

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

dermatophytes
molecular epidemiology
taxonomy
biochemistry and virulence factors
host response
resistance mechanisms

Published Papers (10 papers)

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Research

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8 pages, 435 KiB

Open AccessArticle

Effect of Household Laundering, Heat Drying, and Freezing on the Survival of Dermatophyte Conidia

by Mohammad Akhoundi, Jade Nasrallah, Anthony Marteau, Dahlia Chebbah, Arezki Izri and Sophie Brun

J. Fungi 2022, 8(5), 546; https://doi.org/10.3390/jof8050546 - 23 May 2022

Cited by 3 | Viewed by 2586

Abstract

Dermatomycoses are one of the most common dermatological infectious diseases. Dermatophytoses, such as tinea pedis (athlete’s foot) in adults and tinea capitis in children, are the most prevalent fungal diseases caused by dermatophytes. The transmission of anthropophilic dermatophytoses occurs almost exclusively through indirect contact with patient-contaminated belongings or environments and, subsequently, facilitates the spread of the infection to others. Hygienic measures were demonstrated to have an important role in removing or reducing the fungal burden. Herein, we evaluated the effectiveness of physical-based methods of laundering, heat drying, and freezing in the elimination of Trichophyton tonsurans, T. rubrum, and T. interdigitale conidia in diverse temperatures and time spectra. Based on our findings, laundering at 60 °C was effective for removing the dermatophyte conidia from contaminated linens. On the contrary, heat drying using domestic or laundromat machines; freezing at −20 °C for 24 h, 48 h, or one week; and direct heat exposure at 60 °C for 10, 30, or 90 min were unable to kill the dermatophytes. These results can be helpful for clinicians, staff of children’s communities, and hygiene practitioners for implementing control management strategies against dermatophytoses caused by mentioned dermatophyte species. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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12 pages, 1639 KiB

Open AccessArticle

Terbinafine Resistance in Dermatophytes: A French Multicenter Prospective Study

by Alicia Moreno-Sabater, Anne-Cécile Normand, Anne-Laure Bidaud, Geneviève Cremer, Françoise Foulet, Sophie Brun, Christine Bonnal, Nawel Aït-Ammar, Arnaud Jabet, Aymen Ayachi, Renaud Piarroux, Françoise Botterel, Sandrine Houzé, Guillaume Desoubeaux, Christophe Hennequin and Eric Dannaoui

J. Fungi 2022, 8(3), 220; https://doi.org/10.3390/jof8030220 - 23 Feb 2022

Cited by 33 | Viewed by 3035

Abstract

In recent years, we have moved from the sporadic description of terbinafine-resistant (TerR) Trichophyton spp. isolates to the Indian outbreak due to T. indotineae. Population flows have spread TerR worldwide, altering local epidemiology. We conducted a prospective multicentric study to determine the relative frequency of TerR isolates in France (Paris area) and of the newly introduced T. indotineae species. TerR isolates were screened by the terbinafine-containing-agar-medium (TCAM) method and confirmed by EUCAST. Sequencing methods were used to identify isolates to the species/genotype level and to analyze substitutions in the squalene epoxidase gene (SQLE). In total, 3 isolates out of 580 (T. rubrumn = 1; T. interdigitalen = 1; T. indotineaen = 1) grew on TCAM, showed terbinafine resistance by EUCAST and harbored the Phe397Leu (n = 2) or Leu393Ser (n = 1) substitution in the SQLE. ITS-sequencing of isolates of the T. mentagrophytes/interdigitale complex (n = 125) revealed a relative frequency of 4.8% for T. indotineae and the presence of T. mentagrophytes genotype VII. Despite the detection of terbinafine resistance, isolates from this complex remained susceptible to itraconazole, voriconazole and amorolfine. Terbinafine resistance is present in France and the dermatophyte epidemiology is changing. Efficient systems must be implemented to survey the evolution of newly introduced species and to identify TerR isolates. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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10 pages, 539 KiB

Open AccessArticle

Investigations upon the Improvement of Dermatophyte Identification Using an Online Mass Spectrometry Application

by Arnaud Jabet, Anne-Cécile Normand, Alicia Moreno-Sabater, Jacques Guillot, Veronica Risco-Castillo, Sophie Brun, Magalie Demar, Romain Blaizot, Cécile Nabet, Ann Packeu and Renaud Piarroux

J. Fungi 2022, 8(1), 73; https://doi.org/10.3390/jof8010073 - 11 Jan 2022

Cited by 3 | Viewed by 1686

Abstract

Online MALDI-TOF mass spectrometry applications, such as MSI-2, have been shown to help identify dermatophytes, but recurrent errors are still observed between phylogenetically close species. The objective of this study was to assess different approaches to reduce the occurrence of such errors by adding new reference spectra to the MSI-2 application. Nine libraries were set up, comprising an increasing number of spectra obtained from reference strains that were submitted to various culture durations on two distinct culture media: Sabouraud gentamicin chloramphenicol medium and IDFP Conidia medium. The final library included spectra from 111 strains of 20 species obtained from cultures on both media collected every three days after the appearance of the colony. The performance of each library was then analyzed using a cross-validation approach. The spectra acquisitions were carried out using a Microflex Bruker spectrometer. Diversifying the references and adding spectra from various culture media and culture durations improved identification performance. The percentage of correct identification at the species level rose from 63.4 to 91.7% when combining all approaches. Nevertheless, residual confusion between close species, such as Trichophyton rubrum, Trichophyton violaceum and Trichophyton soudanense, remained. To distinguish between these species, mass spectrometry identification should take into account basic morphological and/or clinico-epidemiological features. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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19 pages, 4493 KiB

Open AccessArticle

Towards a Standardized Procedure for the Production of Infective Spores to Study the Pathogenesis of Dermatophytosis

by Emilie Faway, Cindy Staerck, Célya Danzelle, Sophie Vroomen, Christel Courtain, Bernard Mignon and Yves Poumay

J. Fungi 2021, 7(12), 1029; https://doi.org/10.3390/jof7121029 - 30 Nov 2021

Cited by 1 | Viewed by 2235

Abstract

Dermatophytoses are superficial infections of human and animal keratinized tissues caused by filamentous fungi named dermatophytes. Because of a high and increasing incidence, as well as the emergence of antifungal resistance, a better understanding of mechanisms involved in adhesion and invasion by dermatophytes is required for the further development of new therapeutic strategies. In the last years, several in vitro and in vivo models have emerged to study dermatophytosis pathogenesis. However, the procedures used for the growth of fungi are quite different, leading to a highly variable composition of inoculum for these models (microconidia, arthroconidia, hyphae), thus rendering difficult the global interpretation of observations. We hereby optimized growth conditions, including medium, temperature, atmosphere, and duration of culture, to improve the sporulation and viability and to favour the production of arthroconidia of several dermatophyte species, including Trichophyton rubrum and Trichophyton benhamiae. The resulting suspensions were then used as inoculum to infect reconstructed human epidermis in order to validate their ability to adhere to and to invade host tissues. By this way, this paper provides recommendations for dermatophytes culture and paves the way towards a standardized procedure for the production of infective spores usable in in vitro and in vivo experimental models. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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13 pages, 1588 KiB

Open AccessArticle

Real-Time PCR Assay for the Detection of Dermatophytes: Comparison between an In-House Method and a Commercial Kit for the Diagnosis of Dermatophytoses in Patients from Dakar, Senegal

by Jihane Kabtani, Khadim Diongue, Jean-Noël Dione, Anne Delmas, Coralie L’Ollivier, Marie-Claude Amoureux, Daouda Ndiaye and Stéphane Ranque

J. Fungi 2021, 7(11), 949; https://doi.org/10.3390/jof7110949 - 10 Nov 2021

Cited by 5 | Viewed by 2379

Abstract

Background. PCR assays have been developed for the diagnosis of dermatophytes, yet data in African populations are scarce. Objective. This study aimed to compare two PCR assays for the diagnosis of dermatophytosis in outpatients at the Aristide Le Dantec University Hospital in Dakar, Senegal. Patients and methods. A total of 105 samples, including 24 skin, 19 nail and 62 hair samples collected from 99 patients were included in this study. Each sample was subjected to conventional diagnosis (CD), including direct microscopy and culture, and two real-time PCR assays: one in-house (IH)-PCR, used at the University Hospital of Marseille and the Eurobio Scientific commercial kit (CK): designed for the specific detection of six dermatophytes not including Microsporum audouinii. Results. Of the 105 specimens, 24.8%, 36.2% and 20% were positive by CD, IH-PCR and CK-PCR, respectively. The IH-PCR and CK-PCR exhibited 88.9% and 65.4% sensitivity, respectively. With a 36.6 diagnostic odd ratio and 1.41 needed to diagnose, the IH-PCR displayed better diagnostic indices than the CK-PCR. It is notable that, when considering the species that it claims to detect, when it came to skin and nail samples, CK-PCR sensitivity increased to 77%. Conclusions. The pan-dermatophyte IH-PCR performed better in the diagnosis of dermatophytosis in this African population than the CK-PCR, which is not designed to detect M. audouinii. Nevertheless, both assays exhibited similarly good diagnostic indices for tinea corporis and tinea unguium, both of which are localisations where M. audouinii is more rarely involved than in tinea capitis. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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15 pages, 2119 KiB

Open AccessArticle

An Outbreak of Trichophyton quinckeanum Zoonotic Infections in the Czech Republic Transmitted from Cats and Dogs

by Pavlína Lysková, Radim Dobiáš, Adéla Čmoková, Miroslav Kolařík, Petr Hamal, Kateřina Šmatláková, Jan Hušek, Karel Mencl, Nad’a Mallátová, Zora Poláčková, Anežka Krnáčová, Kristýna Palkovičová, Daniela Jablonská, Jitka Macháčová, Zdeněk Drlík, Denisa Bázsóová, Pavla Jaworská, Lucie Svobodová and Vit Hubka

J. Fungi 2021, 7(9), 684; https://doi.org/10.3390/jof7090684 - 25 Aug 2021

Cited by 13 | Viewed by 3102

Abstract

Trichophyton quinckeanum, a zoophilic dermatophyte mostly known as the causative agent of rodent favus, is relatively rarely reported to cause human infections. Indeed, no infections were detected in Czechia between 2012 and 2015 despite routine verification of species identification by ITS rDNA sequencing. By contrast, 25 human and 11 animal cases of infection were documented from December 2016 to December 2020 and the rates tended to grow every following year. Interestingly, most of the cases were reported in the Olomouc region, suggesting a local outbreak. We bring the evidence that human T. quinckeanum infections are most commonly contracted from infected cats or, less frequently, dogs. Although rodents or contaminated soil and environment could be the source of infection to cats and dogs, the occurrence of infections in multiple animals in the same household suggests direct transmission among animals. Confirmation of the identification by molecular methods is highly recommended due to morphological similarity with T. mentagrophytes/T. interdigitale. Antifungal susceptibility testing of isolates to eight antifungals was performed using EUCAST methodology (E.Def 11.0). Among the tested antifungals, terbinafine, amorolfine, ciclopirox and efinaconazole were most potent in vitro and elevated minimum inhibitory concentrations were obtained for fluconazole and ketoconazole. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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12 pages, 2508 KiB

Open AccessArticle

A Polyphasic Approach to Classification and Identification of Species within the Trichophyton benhamiae Complex

by Frederik Baert, Paulien Lefevere, Elizabet D’hooge, Dirk Stubbe and Ann Packeu

J. Fungi 2021, 7(8), 602; https://doi.org/10.3390/jof7080602 - 26 Jul 2021

Cited by 8 | Viewed by 2533

Abstract

In recent years, considerable advances have been made in clearing up the phylogenetic relationships within the Arthrodermataceae family. However, certain closely related taxa still contain poorly resolved species boundaries. Here, we tried to elucidate the species composition of the Trichophyton benhamiae species complex using a combined approach consisting of multi-gene phylogenetic analysis based on internal transcribed spacer (ITS) and beta-tubulin (BT) gene regions, morphological analysis, and spectral comparison using MALDI-ToF. We confirmed the existence of 11 different monophyletic clades within the complex representing either species or genetically distinct groups within species. MALDI-ToF spectrometry analysis revealed that most of these clades were readily distinguishable from one another; however, some closely related sister clades, such as T. europaeum and T. japonicum, were often misidentified as their counterpart. The distinct “yellow” and “white” phenotypes of T. benhamiae do not have a clear genetic basis and should thus be considered as different morphotypes of the same species. Strains traditionally considered T. benhamiae can be divided into three main clades: (i) T. benhamiae, (ii) T. europaeum/T. japonicum, and (iii) the phylogenetically distant T. africanum. While T. europaeum and T. japonicum are distinguishable based on their genotype, spectral and morphological analysis did not provide clear delimiting characteristics. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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14 pages, 3546 KiB

Open AccessArticle

MFS1, a Pleiotropic Transporter in Dermatophytes That Plays a Key Role in Their Intrinsic Resistance to Chloramphenicol and Fluconazole

by Tsuyoshi Yamada, Takashi Yaguchi, Karine Salamin, Emmanuella Guenova, Marc Feuermann and Michel Monod

J. Fungi 2021, 7(7), 542; https://doi.org/10.3390/jof7070542 - 07 Jul 2021

Cited by 7 | Viewed by 2463

Abstract

A recently identified Trichophyton rubrum major facilitator superfamily (MFS)-type transporter (TruMFS1) has been shown to give resistance to azole compounds and cycloheximide (CYH) when overexpressed in Saccharomyces cerevisiae. We investigated the roles of MFS1 in the intrinsic resistance of dermatophytes to CYH and chloramphenicol (CHL), which are commonly used to isolate these fungi, and to what extent MFS1 affects the susceptibility to azole antifungals. Susceptibility to antibiotics and azoles was tested in S. cerevisiae overexpressing MFS1 and ΔMFS1 mutants of Trichophyton benhamiae, a dermatophyte that is closely related to T. rubrum. We found that TruMFS1 functions as an efflux pump for CHL in addition to CYH and azoles in S. cerevisiae. In contrast, the growth of T. benhamiae ΔMFS1 mutants was not reduced in the presence of CYH but was severely impaired in the presence of CHL and thiamphenicol, a CHL analog. The suppression of MFS1 in T. benhamiae also increased the sensitivity of the fungus to fluconazole and miconazole. Our experiments revealed a key role of MFS1 in the resistance of dermatophytes to CHL and their high minimum inhibitory concentration for fluconazole. Suppression of MFS1 did not affect the sensitivity to CYH, suggesting that another mechanism was involved in resistance to CYH in dermatophytes. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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10 pages, 1008 KiB

Open AccessArticle

Diversity of Geophilic Dermatophytes Species in the Soils of Iran; The Significant Preponderance of Nannizzia fulva

by Simin Taghipour, Mahdi Abastabar, Fahimeh Piri, Elham Aboualigalehdari, Mohammad Reza Jabbari, Hossein Zarrinfar, Sadegh Nouripour-Sisakht, Rasoul Mohammadi, Bahram Ahmadi, Saham Ansari, Farzad Katiraee, Farhad Niknejad, Mojtaba Didehdar, Mehdi Nazeri, Koichi Makimura and Ali Rezaei-Matehkolaei

J. Fungi 2021, 7(5), 345; https://doi.org/10.3390/jof7050345 - 28 Apr 2021

Cited by 10 | Viewed by 2539

Abstract

A molecular epidemiology study was conducted between 2016 and 2017 by a network of collaborators from 12 provinces in the Islamic Republic of Iran. A total of 1484 soil samples from different habitats were screened for the presence of dermatophytes by using the hair baiting technique. The primary identification of isolates was carried out by amplification and MvaI restriction fragment length polymorphism (RFLP) of the internal transcribed spacers regions of ribosomal DNA (ITS-rDNA). The identifications, especially in the cases of isolates with unknown RFLP patterns, were confirmed by sequencing of the ITS-rDNA region. As a result, 256 isolates were recovered. The isolation rate was higher in soils with pH range 7.1–8.0, collected from animal habitats (n = 78; 34%) and parks and gardens (n = 75; 32%), geographically from Mazandaran Province (n = 115; 49.5%) and seasonally in the spring (n = 129; 50.4%), all of which were statistically significant (p < 0.05). The dermatophytes comprising five species of the two genera, viz., Nannizzia fulva (n = 214), N. gypsea (n = 34), Arthroderma quadrifidum (n = 5), A. gertleri (n = 2) and A. tuberculatum (n = 1), were isolated. The geophilic dermatophytes occurred in various soils from different parts of Iran; however, surprisingly, N. fulva emerged as the dominant species, outnumbering the common geophilic species of N. gypsea. For the definitive identification of soil inhabitant dermatophytes, DNA-based identification is strongly recommended. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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Review

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17 pages, 1832 KiB

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State-of-the-Art Dermatophyte Infections: Epidemiology Aspects, Pathophysiology, and Resistance Mechanisms

by Nilce M. Martinez-Rossi, Nalu T. A. Peres, Tamires A. Bitencourt, Maíra P. Martins and Antonio Rossi

J. Fungi 2021, 7(8), 629; https://doi.org/10.3390/jof7080629 - 03 Aug 2021

Cited by 37 | Viewed by 8013

Abstract

The burden of fungal infections is not widely appreciated. Although these infections are responsible for over one million deaths annually, it is estimated that one billion people are affected by severe fungal diseases. Mycoses of nails and skin, primarily caused by fungi known as dermatophytes, are the most common fungal infections. Trichophyton rubrum appears to be the most common causative agent of dermatophytosis, followed by Trichophyton interdigitale. An estimated 25% of the world’s population suffers from dermatomycosis. Although these infections are not lethal, they compromise the quality of life of infected patients. The outcome of antidermatophytic treatments is impaired by various conditions, such as resistance and tolerance of certain dermatophyte strains. The adage “know your enemy” must be the focus of fungal research. There is an urgent need to increase awareness about the significance of these infections with precise epidemiological data and to improve knowledge regarding fungal biology and pathogenesis, with an emphasis on adaptive mechanisms to tackle adverse conditions from host counteractions. This review outlines the current knowledge about dermatophyte infections, with a focus on signaling pathways required for fungal infection establishment and a broad perspective on cellular and molecular factors involved in antifungal resistance and tolerance. Full article

(This article belongs to the Special Issue Epidemiology and Pathogenesis of Dermatophytes)

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