Resolving Phylogenetic Relationships Within the Trichophyton mentagrophytes Complex: A RADseq Genomic Approach Challenges Status of 'Terbinafine-Resistant' Trichophyton indotineae as Distinct Species
Jazyk angličtina Země Německo Médium print
Typ dokumentu časopisecké články
Grantová podpora
61388971
Czech Academy of Sciences, Long term Research Development Project
VP33
Academy of Sciences, Strategy AV21, 'Mycolife - the world of fungi'
NU21-05-00681
Czech Ministry of Health
PubMed
40183506
PubMed Central
PMC11970228
DOI
10.1111/myc.70050
Knihovny.cz E-zdroje
- Klíčová slova
- Trichophyton interdigitale, Trichophyton mentagrophytes, anthropophilic dermatophytes, antifungal resistance, dermatophytosis, population structure, taxonomy, zoophilic dermatophytes,
- MeSH
- antifungální látky * farmakologie MeSH
- Arthrodermataceae * genetika klasifikace účinky léků MeSH
- DNA fungální genetika MeSH
- fylogeneze * MeSH
- genomika metody MeSH
- genotyp MeSH
- jednonukleotidový polymorfismus MeSH
- lidé MeSH
- sekvenční analýza DNA MeSH
- tinea mikrobiologie MeSH
- Trichophyton * genetika klasifikace účinky léků MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- antifungální látky * MeSH
- DNA fungální MeSH
BACKGROUND: The Trichophyton mentagrophytes complex encompasses common dermatophytes causing superficial mycoses in humans and animals. The taxonomy of the complex is unstable, with conflicting views on the species status of some taxa, particularly T. indotineae and T. interdigitale. Due to the presence of intermediate genotypes, neither MALDI-TOF MS nor ITS rDNA sequencing can accurately distinguish all taxa in the complex, potentially contributing to clinical misdiagnoses. OBJECTIVES: This research resolves phylogenetic relationships within the T. mentagrophytes complex. Based on these data, the taxonomical recommendations are suggested. METHODS: In order to resolve the phylogenetic relationship of the T. mentagrophytes complex, we employed Restriction Site-Associated DNA Sequencing (RADseq) to produce a high-resolution single nucleotide polymorphism (SNP) dataset from 95 isolates. The SNP-based analyses indicated the presence of two major genetic clusters corresponding to T. mentagrophytes (including T. indotineae) and T. interdigitale. RESULTS: Our results challenge the species status of T. indotineae because of insufficient genetic divergence from T. mentagrophytes. Therefore, we propose designating T. indotineae as T. mentagrophytes var. indotineae (or T. mentagrophytes ITS genotype VIII) to avoid further splitting of the complex and taxonomic inflation. Although T. interdigitale shows clearer genetic differentiation, its separation is incomplete and identification of some isolates is ambiguous when using routine methods, leading us to consider it a variety as well: T. mentagrophytes var. interdigitale. CONCLUSIONS: We recommend using T. mentagrophytes as the overarching species name for all complex isolates. Where precise molecular identification is possible, the use of variety ranks is encouraged. Since identical resistance mechanisms are not specific to any genotype or dermatophyte species, identifying antifungal resistance is more important than differentiating closely related genotypes or populations.
Department of Botany Faculty of Science Charles University Prague Czech Republic
Department of Genetics and Microbiology Faculty of Science Charles University Prague Czech Republic
Faculty of Medicine University of British Columbia Vancouver Canada
LKC School of Medicine Nanyang Technological University Singapore
State Key Laboratory of Mycology Institute of Microbiology Chinese Academy of Sciences Beijing China
Zobrazit více v PubMed
Summerbell R. C., Weitzman I., and Padhye A. A., Trichopyton, Microsporum, Epidermophyton and Agents of Superficial Mycoses, vol. 2, 9th ed. (ASM Press, 2007).
Havlickova B., Czaika V. A., and Friedrich M., “Epidemiological Trends in Skin Mycoses Worldwide,” Mycoses 51 (2008): 2–15. PubMed
Chowdhary A., Singh A., Singh P. K., Khurana A., and Meis J. F., “Perspectives on Misidentification of Trichophyton interdigitale/Trichophyton mentagrophytes Using Internal Transcribed Spacer Region Sequencing: Urgent Need to Update the Sequence Database,” Mycoses 62 (2019): 11–15. PubMed
Cafarchia C., Iatta R., Latrofa M. S., Graser Y., and Otranto D., “Molecular Epidemiology, Phylogeny and Evolution of Dermatophytes,” Infection, Genetics and Evolution 20 (2013): 336–351. PubMed
Svarcova M., Vetrovsky T., Kolarik M., and Hubka V., “Defining the Relationship Between Phylogeny, Clinical Manifestation, and Phenotype for Trichophyton mentagrophytes/interdigitale Complex; a Literature Review and Taxonomic Recommendations,” Medical Mycology 61 (2023): myad042. PubMed PMC
de Hoog G. S., Dukik K., Monod M., et al., “Toward a Novel Multilocus Phylogenetic Taxonomy for the Dermatophytes,” Mycopathologia 182 (2017): 5–31. PubMed PMC
Gräser Y., Kuijpers A. F. A., Presber W., and De Hoog G. S., “Molecular Taxonomy of Trichophyton mentagrophytes and T. tonsurans ,” Medical Mycology 37 (1999): 315–330. PubMed
Nenoff P., Herrmann J., and Graser Y., “ Trichophyton mentagrophytes Sive interdigitale? A Dermatophyte in the Course of Time,” Journal der Deutschen Dermatologischen Gesellschaft 5 (2007): 198–202. PubMed
Beguin H., Pyck N., Hendrickx M., Planard C., Stubbe D., and Detandt M., “The Taxonomic Status of Trichophyton Quinckeanum and T. interdigitale Revisited: A Multigene Phylogenetic Approach,” Medical Mycology 87 (2012): 871–882. PubMed
Kano R., Kimura U., Kakurai M., et al., “ Trichophyton indotineae sp. Nov.: A New Highly Terbinafine‐Resistant Anthropophilic Dermatophyte Species,” Mycopathologia 185 (2020): 947–958. PubMed
Tang C., Kong X., Ahmed S. A., et al., “Taxonomy of the Trichophyton mentagrophytes/T. interdigitale Species Complex Harboring the Highly Virulent, Multiresistant Genotype T. indotineae ,” Mycopathologia 186 (2021): 315–326. PubMed PMC
Uhrlaß S., Verma S. B., Gräser Y., et al., “ Trichophyton indotineae—An Emerging Pathogen Causing Recalcitrant Dermatophytoses in India and Worldwide—A Multidimensional Perspective,” Journal of Fungi 8, no. 7 (2022): 757, 10.3390/jof8070757. PubMed DOI PMC
Parchman T. L., Jahner J. P., Uckele K. A., Galland L. M., and Eckert A. J., “RADseq Approaches and Applications for Forest Tree Genetics,” Tree Genetics & Genomes 14 (2018): 1–25.
Lasalle A., Cáceres P., Montenegro T., Araneda C., Yáñez J., and Vizziano‐Cantonnet D., “Development of a Dense SNP Panel for the Siberian Sturgeon (Acipenser baerii) Using High‐Depth RAD‐Seq,” Conservation Genetics Resources 14 (2021): 37–39.
Martinez J. G., Rangel‐Medrano J. D., Yepes‐Acevedo A. J., Restrepo‐Escobar N., and Marquez E. J., “Species Limits and Introgression in Pimelodus From the Magdalena‐Cauca River Basin,” Molecular Phylogenetics and Evolution 173 (2022): 107517. PubMed
Razkin O., Sonet G., Breugelmans K., Madeira M. J., Gomez‐Moliner B. J., and Backeljau T., “Species Limits, Interspecific Hybridization and Phylogeny in the Cryptic Land Snail Complex Pyramidula: The Power of RADseq Data,” Molecular Phylogenetics and Evolution 101 (2016): 267–278. PubMed
Sain M. P., Norrell‐Tober J., Barthel K., et al., “Multiple Complementary Studies Clarify Which Co‐Occurring Congener Presents the Greatest Hybridization Threat to a Rare Texas Endemic Wildflower (Hibiscus dasycalyx: Malvaceae),” Journal of the Botanical Research Institute of Texas 15 (2021): 283–308.
Wagner H. C., Gamisch A., Arthofer W., Moder K., Steiner F. M., and Schlick‐Steiner B. C., “Evolution of Morphological Crypsis in the Tetramorium caespitum Ant Species Complex (Hymenoptera: Formicidae),” Scientific Reports 8 (2018): 12547. PubMed PMC
Zerbino D. R. and Birney E., “Velvet: Algorithms for de Novo Short Read Assembly Using de Bruijn Graphs,” Genome Research 18 (2008): 821–829. PubMed PMC
Langmead B., Trapnell C., Pop M., and Salzberg S. L., “Ultrafast and Memory‐Efficient Alignment of Short DNA Sequences to the Human Genome,” Genome Biology 10 (2009): 1–10. PubMed PMC
Li H., “Aligning Sequence Reads, Clone Sequences and Assembly Contigs With BWA‐MEM,” arXiv, (2013), 10.48550/arXiv.1303.3997. DOI
Li H., Handsaker B., Wysoker A., et al., “The Sequence Alignment/Map Format and SAMtools,” Bioinformatics 25 (2009): 2078–2079. PubMed PMC
Bradbury P. J., Zhang Z., Kroon D. E., Casstevens T. M., Ramdoss Y., and Buckler E. S., “TASSEL: Software for Association Mapping of Complex Traits in Diverse Samples,” Bioinformatics 23 (2007): 2633–2635. PubMed
Zeisek V., “STRUCTURE Multi PBS Pro Scripts, on github.com,” (2021), accessed January 10, 2021, https://github.com/V‐Z/structure‐multi‐pbspro.git.
Carstens B. C., Pelletier T. A., Reid N. M., and Satler J. D., “How to Fail at Species Delimitation,” Molecular Biology and Evolution 22 (2013): 4369–4383. PubMed
Earl D. A. and Von Holdt B. M., “STRUCTURE HARVESTER: A Website and Program for Visualizing STRUCTURE Output and Implementing the Evanno Method,” Conservation Genetics Resources 4 (2012): 359–361.
Leigh J. W. and Bryant D., “POPART: Full‐Feature Software for Haplotype Network Construction,” Methods in Ecology and Evolution 6 (2015): 1110–1116.
Knaus B. J. and Grünwald N. J., “Vcfr: A Package to Manipulate and Visualize Variant Call Format Data in R,” Molecular Ecology Resources 17 (2017): 44–53. PubMed
Jombart T. and Ahmed I., “Adegenet 1.3‐1: New Tools for the Analysis of Genome‐Wide SNP Data,” Bioinformatics 27 (2011): 3070–3071. PubMed PMC
Wickham H., ggplot2: Elegant Graphics for Data Analysis New York. Applied Spatial Data Analysis (Springer New York, 2009), 784–785.
Bryant D., Bouckaert R., Felsenstein J., Rosenberg N. A., and RoyChoudhury A., “Inferring Species Trees Directly From Biallelic Genetic Markers: Bypassing Gene Trees in a Full Coalescent Analysis,” Molecular Biology and Evolution 29 (2012): 1917–1932. PubMed PMC
Bouckaert R., Vaughan T. G., Barido‐Sottani J., et al., “BEAST 2.5: An Advanced Software Platform for Bayesian Evolutionary Analysis,” PLoS Computational Biology 15 (2019): e1006650. PubMed PMC
Rambaut A., “FigTree,” (2024), accessed November, 12, 2024, http://tree.bio.ed.ac.uk/software/figtree/.
Lanfear R., Frandsen P. B., Wright A. M., Senfeld T., and Calcott B., “PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses,” Molecular Biology and Evolution 34 (2017): 772–773. PubMed
Minh B. Q., Schmidt H. A., Chernomor O., et al., “IQ‐TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era,” Molecular Biology and Evolution 37 (2020): 1530–1534. PubMed PMC
R_Development_Core_Team , “R: A Language and Environment for Statistical Computing,” (2021), Vienna, Austria: R Foundation for Statistical Computing, http://www.R‐project.org.
Paradis E., Claude J., and Strimmer K., “APE: Analyses of Phylogenetics and Evolution in R Language,” Bioinformatics 20 (2004): 289–290. PubMed
Revell L. J., “Phytools: An R Package for Phylogenetic Comparative Biology (And Other Things),” Methods in Ecology and Evolution 3 (2012): 217–223.
Pchelin I. M., Azarov D. V., Churina M. A., et al., “Species Boundaries in the Trichophyton mentagrophytes / T. interdigitale Species Complex,” Medical Mycology 57 (2019): 781–789. PubMed
Tang C., Ahmed S. A., Deng S., et al., “Detection of Emerging Genotypes in Trichophyton mentagrophytes Species Complex: A Proposal for Handling Biodiversity in Dermatophytes,” Frontiers in Microbiology 13 (2022): 960190, 10.3389/fmicb.2022.960190. PubMed DOI PMC
Nenoff P., Uhrlaß S., Verma S. B., and Panda S., “ Trichophyton mentagrophytes ITS Genotype VIII and Trichophyton indotineae: A Terminological Maze, or Is It?,” Indian Journal of Dermatology, Venereology and Leprology 88 (2022): 586–589. PubMed
Shaw D., Singh S., Dogra S., et al., “MIC and Upper Limit of Wild‐Type Distribution for 13 Antifungal Agents Against a Trichophyton mentagrophytes‐Trichophyton interdigitale Complex of Indian Origin,” Antimicrobial Agents and Chemotherapy 64 (2020): e0196419, 10.1128/AAC.01964-19. PubMed DOI PMC
Symoens F., Jousson O., Planard C., et al., “Molecular Analysis and Mating Behaviour of the Trichophyton mentagrophytes Species Complex,” International Journal of Medical Microbiology 301 (2011): 260–266. PubMed
Bontems O., Fratti M., Salamin K., Guenova E., and Monod M., “Epidemiology of Dermatophytoses in Switzerland According to a Survey of Dermatophytes Isolated in Lausanne Between 2001 and 2018,” Journal of Fungi 6 (2020): 1–8. PubMed PMC
Frías‐De‐León M. G., Hernández‐Castro R., Vite‐Garín T., et al., “Antifungal Resistance in Candida auris: Molecular Determinants,” Antibiotics 9, no. 9 (2020): 568. PubMed PMC
de Hoog S., Walsh T. J., Ahmed S. A., et al., “A Conceptual Framework for Nomenclatural Stability and Validity of Medically Important Fungi: A Proposed Global Consensus Guideline for Fungal Name Changes Supported by ABP, ASM, CLSI, ECMM, ESCMID‐EFISG, EUCAST‐AFST, FDLC, IDSA, ISHAM, MMSA, and MSGERC,” Journal of Clinical Microbiology 61 (2023): e00873‐23. PubMed PMC
Normand A.‐C., Moreno‐Sabater A., Jabet A., et al., “MALDI‐TOF Mass Spectrometry Online Identification of Trichophyton indotineae Using the MSI‐2 Application,” Journal of Fungi 8 (2022): 1103. PubMed PMC
Tang C., Zhou X., Guillot J., et al., “Dermatophytes and Mammalian Hair: Aspects of the Evolution of Arthrodermataceae,” Fungal Diversity 125 (2024): 139–156.
Kumar P., Ramachandran S., Das S., Bhattacharya S., and Taneja B., “Insights Into Changing Dermatophyte Spectrum in India Through Analysis of Cumulative 161,245 Cases Between 1939 and 2021,” Mycopathologia 188 (2023): 1–20. PubMed PMC
Alshahni M. M., Yamada T., Yo A., et al., “Insight Into the Draft Whole‐Genome Sequence of the Dermatophyte Arthroderma vanbreuseghemii ,” Scientific Reports 8 (2018): 15127, 10.1038/s41598-018-33505-9. PubMed DOI PMC
Persinoti G. F., Martinez D. A., Li W., et al., “Whole‐Genome Analysis Illustrates Global Clonal Population Structure of the Ubiquitous Dermatophyte Pathogen Trichophyton rubrum ,” Genetics 208 (2018): 1657–1669. PubMed PMC
Singh A., Masih A., Monroy‐Nieto J., et al., “A Unique Multidrug‐Resistant Clonal Trichophyton Population Distinct From Trichophyton mentagrophytes/Trichophyton interdigitale Complex Causing an Ongoing Alarming Dermatophytosis Outbreak in India: Genomic Insights and Resistance Profile,” Fungal Genetics and Biology 133 (2019): 103266, 10.1016/j.fgb.2019.103266. PubMed DOI
Gräser Y., Fröhlich J., Presber W., and de Hoog S., “Microsatellite Markers Reveal Geographic Population Differentiation in Trichophyton rubrum ,” Journal of Medical Microbiology 56 (2007): 1058–1065. PubMed
Ohst T., De Hoog S., Presber W., Stavrakieva V., and Graser Y., “Origins of Microsatellite Diversity in the Trichophyton rubrum‐T. violaceum Clade (Dermatophytes),” Journal of Clinical Microbiology 42 (2004): 4444–4448. PubMed PMC
Čmoková A., Kolařík M., Dobiáš R., et al., “Resolving the Taxonomy of Emerging Zoonotic Pathogens in the Trichophyton Benhamiae Complex,” Fungal Diversity 104 (2020): 333–387.
Čmoková A., Kolařík M., Guillot J., et al., “Host‐Driven Subspeciation in the Hedgehog Fungus, Trichophyton erinacei, an Emerging Cause of Human Dermatophytosis,” Persoonia 48 (2022): 203–218. PubMed PMC
Čmoková A., Rezaei‐Matehkolaei A., Kuklová I., et al., “Discovery of New Trichophyton Members, T. persicum and T. spiraliforme spp. Nov., as a Cause of Highly Inflammatory Tinea Cases in Iran and Czechia,” Microbiology Spectrum 9 (2021): e00284‐21. PubMed PMC
Aneke C. I., Čmoková A., Hubka V., Rhimi W., Otranto D., and Cafarchia C., “Subtyping Options for Microsporum canis Using Microsatellites and MLST: A Case Study From Southern Italy,” Pathogens 11 (2021): e10004, 10.3390/pathogens11010004. PubMed DOI PMC
Pasquetti M., Peano A., Soglia D., et al., “Development and Validation of a Microsatellite Marker‐Based Method for Tracing Infections by Microsporum canis ,” Journal of Dermatological Science 70 (2013): 123–129. PubMed
Mochizuki T., Futatsuya T., Anzawa K., et al., “Multilocus Microsatellite Analysis of the Molecular Epidemiology of Microsporum canis Isolated in Japan,” Medical Mycology Journal 64 (2023): 63–72. PubMed
Pchelin I. M., Zlatogursky V. V., Rudneva M. V., et al., “Reconstruction of Phylogenetic Relationships in Dermatomycete Genus Trichophyton Malmsten 1848 Based on Ribosomal Internal Transcribed Spacer Region, Partial 28S rRNA and Beta‐Tubulin Genes Sequences,” Mycoses 59 (2016): 566–575. PubMed
Woudenberg J., Seidl M., Groenewald J., et al., “ Alternaria Section Alternaria: Species, Formae Speciales or Pathotypes?,” Studies in Mycology 82 (2015): 1–21. PubMed PMC
Sklenar F., Glassnerova K., Jurjevic Z., et al., “Taxonomy of Aspergillus Series versicolores: Species Reduction and Lessons Learned About Intraspecific Variability,” Studies in Mycology 102 (2022): 53–93. PubMed PMC
Bian C., Kusuya Y., Sklenář F., et al., “Reducing the Number of Accepted Species in Aspergillus Series Nigri ,” Studies in Mycology 102 (2022): 95–132. PubMed PMC
Boluda C. G., Rico V., Divakar P., et al., “Evaluating Methodologies for Species Delimitation: The Mismatch Between Phenotypes and Genotypes in Lichenized Fungi (Bryoria Sect. Implexae, Parmeliaceae),” Persoonia 42 (2019): 75–100. PubMed PMC
Hilário S., Gonçalves M. F., and Alves A., “Using Genealogical Concordance and Coalescent‐Based Species Delimitation to Assess Species Boundaries in the Diaporthe eres Complex,” Journal of Fungi 7 (2021): 507, 10.3390/jof7070507. PubMed DOI PMC
Wang P. M., Liu X. B., Dai Y. C., Horak E., Steffen K., and Yang Z. L., “Phylogeny and Species Delimitation of Flammulina: Taxonomic Status of Winter Mushroom in East Asia and a New European Species Identified Using an Integrated Approach,” Mycological Progress 17 (2018): 1013–1030.
Singh A., Masih A., Khurana A., et al., “High Terbinafine Resistance in Trichophyton interdigitale Isolates in Delhi, India Harbouring Mutations in the Squalene Epoxidase Gene,” Mycoses 61 (2018): 477–484. PubMed
Kolarczyková D., Lysková P., Švarcová M., et al., “Terbinafine Resistance in Trichophyton mentagrophytes and Trichophyton rubrum in The Czech Republic: A Prospective Multicentric Study,” Mycoses 67 (2024): e13708. PubMed
Rudramurthy S. M., Shankarnarayan S. A., Dogra S., et al., “Mutation in the Squalene Epoxidase Gene of Trichophyton interdigitale and Trichophyton rubrum Associated With Allylamine Resistance,” Antimicrobial Agents and Chemotherapy 62 (2018): e02522‐17, 10.1128/aac.02522-17. PubMed DOI PMC
Kano R., Kimura U., Noguchi H., and Hiruma M., “Clinical Isolate of a Multi‐Antifungal‐Resistant Trichophyton rubrum ,” Antimicrobial Agents and Chemotherapy 66 (2022): e02393‐21. PubMed PMC
Osborne C. S., Leitner I., Favre B., and Ryder N. S., “Amino Acid Substitution in Trichophyton rubrum Squalene Epoxidase Associated With Resistance to Terbinafine,” Antimicrobial Agents and Chemotherapy 49 (2005): 2840–2844. PubMed PMC
Mahmood H. R., Shams‐Ghahfarokhi M., Salehi Z., and Razzaghi‐Abyaneh M., “Epidemiological Trends, Antifungal Drug Susceptibility and SQLE Point Mutations in Etiologic Species of Human Dermatophytosis in Al‐Diwaneyah, Iraq,” Scientific Reports 14 (2024): 12669. PubMed PMC
Siopi M., Efstathiou I., Theodoropoulos K., Pournaras S., and Meletiadis J., “Molecular Epidemiology and Antifungal Susceptibility of Trichophyton Isolates in Greece: Emergence of Terbinafine‐Resistant Trichophyton mentagrophytes Type VIII Locally and Globally,” Journal of Fungi 7 (2021): 419. PubMed PMC
Blanchard G., Amarov B., Fratti M., et al., “Reliable and Rapid Identification of Terbinafine Resistance in Dermatophytic Nail and Skin Infections,” Journal of the European Academy of Dermatology and Venereology 37 (2023): 2080–2089. PubMed
Cañete‐Gibas C. F., Mele J., Patterson H. P., et al., “Terbinafine‐Resistant Dermatophytes and the Presence of Trichophyton indotineae in North America,” Journal of Clinical Microbiology 61 (2023): e00562‐23. PubMed PMC
Moreno‐Sabater A., Normand A. C., Bidaud A. L., et al., “Terbinafine Resistance in Dermatophytes: A French Multicenter Prospective Study,” Journal of Fungi 8 (2022): 220. PubMed PMC
Nenoff P., Verma S. B., Ebert A., et al., “Spread of Terbinafine‐Resistant Trichophyton mentagrophytes Type VIII (India) in Germany–‘the Tip of the Iceberg?’,” Journal of Fungi 6 (2020): 1–20. PubMed PMC
Ngo T. M. C., Santona A., Ton Nu P. A., et al., “Detection of Terbinafine‐Resistant Trichophyton indotineae Isolates Within the Trichophyton mentagrophytes Species Complex Isolated From Patients in Hue City, Vietnam: A Comprehensive Analysis,” Medical Mycology 62 (2024): myae088. PubMed
Kong X., Tang C., Singh A., et al., “Antifungal Susceptibility and Mutations in the Squalene Epoxidase Gene in Dermatophytes of the Trichophyton mentagrophytes Species Complex,” Antimicrobial Agents and Chemotherapy 65 (2021): e0005621. PubMed PMC
Ebert A., Monod M., Salamin K., et al., “Alarming India‐Wide Phenomenon of Antifungal Resistance in Dermatophytes: A Multicentre Study,” Mycoses 63 (2020): 717–728. PubMed
Mohammadi L. Z., Shams‐Ghahfarokhi M., Salehi Z., and Razzaghi‐Abyaneh M., “Increased Terbinafine Resistance Among Clinical Genotypes of Trichophyton mentagrophytes/T. interdigitale Species Complex Harboring Squalene Epoxidase Gene Mutations,” Journal of Medical Mycology 34 (2024): 101495. PubMed
Fan X., Dai R.‐C., Zhang S., et al., “Tandem Gene Duplications Contributed to High‐Level Azole Resistance in a Rapidly Expanding Candida tropicalis Population,” Nature Communications 14 (2023): 8369. PubMed PMC
Rhodes J., Abdolrasouli A., Dunne K., et al., “Population Genomics Confirms Acquisition of Drug‐Resistant Aspergillus fumigatus Infection by Humans From the Environment,” Nature Microbiology 7 (2022): 663–674. PubMed PMC
Etienne K. A., Berkow E. L., Gade L., et al., “Genomic Diversity of Azole‐Resistant Aspergillus fumigatus in the United States,” MBio 12, no. 4 (2021): e0180321, 10.1128/mBio.01803-21. PubMed DOI PMC
Heidemann S., Monod M., and Graser Y., “Signature Polymorphisms in the Internal Transcribed Spacer Region Relevant for the Differentiation of Zoophilic and Anthropophilic Strains of Trichophyton interdigitale and Other Species of T. mentagrophytes Sensu Lato ,” British Journal of Dermatology 162 (2010): 282–295. PubMed
Dhib I., Khammari I., Yaacoub A., et al., “Relationship Between Phenotypic and Genotypic Characteristics of Trichophyton mentagrophytes Strains Isolated From Patients With Dermatophytosis,” Mycopathologia 182 (2017): 487–493. PubMed
Taghipour S., Pchelin I. M., Zarei Mahmoudabadi A., et al., “ Trichophyton mentagrophytes and T. interdigitale Genotypes Are Associated With Particular Geographic Areas and Clinical Manifestations,” Mycoses 62 (2019): 1084–1091. PubMed
Klinger M., Theiler M., and Bosshard P., “Epidemiological and Clinical Aspects of Trichophyton mentagrophytes/Trichophyton interdigitale Infections in the Zurich Area: A Retrospective Study Using Genotyping,” Journal of the European Academy of Dermatology and Venereology 35 (2021): 1017–1025. PubMed
Jabet A., Dellière S., Seang S., et al., “Sexually Transmitted Trichophyton mentagrophytes Genotype VII Infection Among Men Who Have Sex With Men,” Emerging Infectious Diseases 29 (2023): 1411. PubMed PMC
Rudramurthy S. M., Shaw D., Shankarnarayan S. A., Abhishek, and Dogra S., “Comprehensive Taxonomical Analysis of Trichophyton mentagrophytes/interdigitale Complex of Human and Animal Origin From India,” Journal of Fungi 9, no. 5 (2023): 577. PubMed PMC
Kumar M. N., Thomas P., A V., et al., “Molecular Epidemiology of Trichophyton Infections Among Canines From Northern India,” Journal of Medical Mycology 33, no. 1 (2022): 101352. PubMed
Oladzad V., Omran A. N., Haghani I., Nabili M., Seyedmousavi S., and Hedayati M. T., “Multi‐Drug Resistance Trichophyton indotineae in a Stray Dog,” Research in Veterinary Science 166 (2024): 105105. PubMed
Nikkholgh S., Pchelin I. M., Zarei Mahmoudabadi A., et al., “Sheep Serve as a Reservoir of Trichophyton mentagrophytes Genotype V Infection,” Medical Mycology 61 (2023): myad066. PubMed
Kupsch C., Czaika V. A., Deutsch C., and Graser Y., “ Trichophyton mentagrophytes – a New Genotype of Zoophilic Dermatophyte Causes Sexually Transmitted Infections,” Journal der Deutschen Dermatologischen Gesellschaft 17 (2019): 493–501. PubMed
Yamada T., Maeda M., Alshahni M. M., et al., “Terbinafine Resistance of Trichophyton Clinical Isolates Caused by Specific Point Mutations in the Squalene Epoxidase Gene,” Antimicrobial Agents and Chemotherapy 61 (2017): e00115‐17, 10.1128/aac.00115-17. PubMed DOI PMC
Suh S. O., Grosso K. M., and Carrion M. E., “Multilocus Phylogeny of the Trichophyton mentagrophytes Species Complex and the Application of Matrix‐Assisted Laser Desorption/Ionization‐Time‐Of‐Flight (MALDI‐TOF) Mass Spectrometry for the Rapid Identification of Dermatophytes,” Mycologia 110 (2018): 118–130. PubMed
De Paepe R., Normand A.‐C., Uhrlaß S., Nenoff P., Piarroux R., and Packeu A., “Resistance Profile, Terbinafine Resistance Screening and MALDI‐TOF MS Identification of the Emerging Pathogen Trichophyton indotineae ,” Mycopathologia 189 (2024): 29. PubMed PMC
Hainsworth S., Hubka V., Lawrie A. C., Carter D., Vanniasinkam T., and Grando D., “Predominance of Trichophyton interdigitale Revealed in Podiatric Nail Dust Collections in Eastern Australia,” Mycopathologia 185 (2020): 175–185. PubMed
Nenoff P., Verma S. B., Vasani R., et al., “The Current Indian Epidemic of Superficial Dermatophytosis due to Trichophyton mentagrophytes‐A Molecular Study,” Mycoses 62 (2019): 336–356. PubMed
Uhrlaß S., Mey S., Koch D., et al., “Dermatophytes and Skin Dermatophytoses in Southeast Asia—First Epidemiological Survey From Cambodia,” Mycoses 67 (2024): e13718. PubMed