, 166:239 | Cite as

The New Species Concept in Dermatophytes—a Polyphasic Approach

  • Yvonne Gräser
  • James Scott
  • Richard Summerbell


The dermatophytes are among the most frequently observed organisms in biomedicine, yet there has never been stability in the taxonomy, identification and naming of the approximately 25 pathogenic species involved. Since the identification of these species is often epidemiologically and ethically important, the difficulties in dermatophyte identification are a fruitful topic for modern molecular biological investigation, done in tandem with renewed investigation of phenotypic characters. Molecular phylogenetic analyses such as multilocus sequence typing have had to be tailored to accommodate differing the mechanisms of speciation that have produced the dermatophytes that are commonly seen today. Even so, some biotypes that were unambiguously considered species in the past, based on profound differences in morphology and pattern of infection, appear consistently not to be distinct species in modern molecular analyses. Most notable among these are the cosmopolitan bane of nails and feet, Trichophyton rubrum, and the endemic African agent of childhood tinea capitis, Trichophyton soudanense, which are effectively inseparable in all analyses. The molecular data require some reinterpretation of results seen in conventional phenotypic tests, but in most cases, phylogenetic insight is readily integrated with current laboratory testing procedures.


Dermatophytes Taxonomy Molecular identification Morphological identification Species concept 


  1. 1.
    Kane J, Summerbell RC, Sigler L, Krajden S, Land G. Laboratory handbook of dermatophytes. Belmont CA, USA: Star Publishers; 1997.Google Scholar
  2. 2.
    Gupta AK, Hofstader SL, Adam P, Summerbell RC. Tinea capitis: an overview with emphasis on management. Pediatr Dermatol. 1999;16:171–89.PubMedCrossRefGoogle Scholar
  3. 3.
    Rippon JW, Fromting RA. Cutaneous antifungal agents. New York: Dekker; 1993. p. 199–214.Google Scholar
  4. 4.
    Kwon-Chung KJ, Bennett JE. Medical mycology. Philadelphia USA: Lea & Febiger; 1992.Google Scholar
  5. 5.
    Elewski BE, Leyden J, Rinaldi MG, Atillasoy E. Office practice-based confirmation of onychomycosis: a US-nationwide prospective survey. Arch Intern Med. 2002;162:2133–8.PubMedCrossRefGoogle Scholar
  6. 6.
    Arcus KD, Kessel AS. Are medical ethics relative to time and place? Star Wars perspective on the Alder Hey affair. BMJ. 2002;325:1493–5.PubMedCrossRefGoogle Scholar
  7. 7.
    Summerbell RC. What is the evolutionary and taxonomic status of asexual lineages in the dermatophytes? Stud Mycol. 2002;47:97–101.Google Scholar
  8. 8.
    Gräser Y, Kühnisch J, Presber W. Molecular markers reveal exclusively clonal reproduction in Trichophyton rubrum. J Clin Microbiol. 1999;37:3713–7.PubMedGoogle Scholar
  9. 9.
    Gräser Y, Fröhlich J, Presber W, de Hoog GS. Microsatellite markers reveal geographic population differentiation in Trichophyton rubrum. J Med Microbiol. 2007;56:1058–65.PubMedCrossRefGoogle Scholar
  10. 10.
    Gräser Y, de Hoog GS, Summerbell RC. Dermatophytes: recognizing species of clonal fungi. Med Mycol. 2006;44:199–209.PubMedCrossRefGoogle Scholar
  11. 11.
    Malmsten PH. Trichophyton tonsurans, hårskärande mögel. Bidrag till utredande af de sjukdomar, som vålla hårets affall. Stockholm: L.J. Hjerta; 1845.Google Scholar
  12. 12.
    Sabouraud R. Les teignes. Paris: Masson & Co.; 1910.Google Scholar
  13. 13.
    Emmons CW. Dermatophytes. Natural grouping based on the form of the spores and accessory organs. Arch Dermatol Syphilol. 1934;30:337–62.Google Scholar
  14. 14.
    Ajello L, Georg LK. In vitro hair cultures for differentiating between atypical isolates of Trichophyton mentagrophytes and Trichophyton rubrum. Mycopathol Mycol Appl. 1957;8:3–17.PubMedCrossRefGoogle Scholar
  15. 15.
    Georg LK, Camp LB. Routine nutritional tests for the identification of dermatophytes. J Bacteriol. 1957;74:113–21.PubMedCrossRefGoogle Scholar
  16. 16.
    Rosenthal SA, Sokolsky H. Enzymatic studies with pathogenic fungi. Dermatol Int. 1965;4:72–9.PubMedCrossRefGoogle Scholar
  17. 17.
    Philpot C. The differentiation of Trichophyton mentagrophytes from Trichophyton rubrum by a simple urease test. Sabouraudia. 1967;5:189–93.PubMedGoogle Scholar
  18. 18.
    Fischer JB, Kane J. The detection of contamination in Trichophyton rubrum and Trichophyton mentagrophytes. Mycopathol Mycol Appl. 1971;19:169–80.CrossRefGoogle Scholar
  19. 19.
    Summerbell RC, Rosenthal SA, Kane J. Rapid method of differentiation of Trichophyton rubrum, Trichophyton mentagrophytes, and related dermatophyte species. J Clin Microbiol. 1988;26:2279–82.PubMedGoogle Scholar
  20. 20.
    Kane J, Salkin IF, Weitzman I, Smitka C. Trichophyton raubitschekii sp. nov. Mycotaxon. 1981;13:259–66.Google Scholar
  21. 21.
    Padhye AA, Weitzman I, Domenech E. An unusual variant of Trichophyton tonsurans var. sulfureum. J Med Vet Mycol. 1994;32:147–50.PubMedCrossRefGoogle Scholar
  22. 22.
    Dawson CO, Gentles JC. The perfect states of Keratinomyces ajelloi Vanbreuseghem, Trichophyton terrestre Durie and Frey and Microsporum nanum Fuentes. Sabouraudia. 1961;1:49–57.PubMedGoogle Scholar
  23. 23.
    Stockdale PM. Nannizzia incurvata gen. nov., sp. nov., a perfect state of Microsporum gypseum (Bodin) Guiart et Grigorakis. Sabouraudia. 1961;1:41–8.Google Scholar
  24. 24.
    Stockdale PM. Sexual stimulation between Arthroderma simii Stockd., Mackenzie and Austwick and related species. Sabouraudia. 1968;6:176–81.PubMedGoogle Scholar
  25. 25.
    Summerbell RC. Form and function in the evolution of dermatophytes. In: Kushwaha RKS, Guarro J, editors. Biology of dermatophytes and other keratinophilic fungi. Rev Iberoam Micol. 2000;17 Suppl:30–43.Google Scholar
  26. 26.
    Rebell G, Taplin G. Dermatophytes, their identification and recognition. 2nd ed. Miami, FL, USA: University of Miami Press; 1970.Google Scholar
  27. 27.
    Davison FD, Mackenzie DW, Owen RJ. Deoxyribonucleic acid base compositions of dermatophytes. J Gen Microbiol. 1980;118:465–70.PubMedGoogle Scholar
  28. 28.
    Mochizuki T, Uehara M, Menon T, Ranganathan S. Minipreparation of total cellular DNA is useful as an alternative molecular marker of mitochondrial DNA for the identification of Trichophyton mentagrophytes and T. rubrum. Mycoses. 1996;39:31–5.PubMedCrossRefGoogle Scholar
  29. 29.
    Gräser Y, El Fari M, Vilgalys R, Kuijpers AFA, de Hoog GS, Presber W, Tietz HJ. Phylogeny and taxonomy of the family Arthrodermataceae (dermatophytes) using sequence analysis of the ribosomal ITS region. Med Mycol. 1999;37:105–14.PubMedCrossRefGoogle Scholar
  30. 30.
    Gräser Y, Kuipers A, Presber W, de Hoog S. Molecular taxonomy of Trichophyton mentagrophytes and T. tonsurans. Med Mycol. 1999;37:315–30.PubMedCrossRefGoogle Scholar
  31. 31.
    Makimura K, Tamura Y, Mochizuki T, Hasegawa A, Tajiri Y, Hanazawa R, Uchida K, Saito H, Yamaguchi H. Phylogenetic classification and species identification of dermatophyte strains based on DNA sequences of nuclear ribosomal internal transcribed spacer 1 regions. J Clin Microbiol. 1999;37:920–4.PubMedGoogle Scholar
  32. 32.
    Gräser Y, Kuijpers AFA, El Fari M, Presber W, de Hoog GS. Molecular and conventional taxonomy of the Microsporum canis complex. Med Mycol. 2000;38:143–53.PubMedCrossRefGoogle Scholar
  33. 33.
    Gräser Y, de Hoog GS, Kuijpers AFA. Recent advances in the molecular taxonomy of dermatophytes. In: Kushwaha RKS, Guarro J, editors. Biology of dermatophytes and other keratinophilic fungi. Rev Iberoam Micol. 2000;17(Suppl.):17–21.Google Scholar
  34. 34.
    Summerbell RC, Haugland R, Li A, Gupta AK. Ribosomal RNA gene internal transcribed spacer 1 and 2 sequences of asexual, anthropophilic dermatophytes related to Trichophyton rubrum. J Clin Microbiol. 1999;37:4005–11.PubMedGoogle Scholar
  35. 35.
    Kano R, Aihara S, Nakamura Y, Watanabe S, Hasegawa A. Chitin synthase 1 (Chs1) gene sequences of Microsporum equinum and Trichophyton equinum. Vet Microbiol. 2001;78:85–90.PubMedCrossRefGoogle Scholar
  36. 36.
    Summerbell RC, Moore MK, Starink-Willemse M, Van Iperen A. ITS barcodes for Trichophyton tonsurans and T. equinum. Med Mycol. 2007;45:193–200.PubMedCrossRefGoogle Scholar
  37. 37.
    Probst S, de Hoog GS, Gräser Y. Development of DNA markers to explore host shifts in dermatophytes. Stud Mycol. 2003;47:57–74.Google Scholar
  38. 38.
    Kaszubiak A, Klein S, de Hoog GS, Gräser Y. Population structure and evolutionary origins of Microsporum canis, M. ferrugineum and M. audouinii. Inf Gen Evol. 2004;4:179–86.CrossRefGoogle Scholar
  39. 39.
    Summerbell RC, Weitzman I, Padhye A. The Trichophyton mentagrophytes complex: biological species and mating type prevalences of North American isolates, and a review of the worldwide distribution and host associations of species and mating types. Stud Mycol. 2002;47:75–86.Google Scholar
  40. 40.
    Mochizuki T, Watanabe S, Uehara M. Genetic homogeneity of Trichophyton mentagrophytes var. interdigitale isolated from geographically distant regions. J Med Vet Mycol. 1996;34:139–43.PubMedCrossRefGoogle Scholar
  41. 41.
    Vanbreuseghem R. Guide Pratique de Mycologie Médicale et Vétérinaire. Paris: Masson & Co.; 1966.Google Scholar
  42. 42.
    Summerbell RC, Li A, Haugland R. What constitutes a functional species in the asexual dermatophytes? Microbiol Cult Coll. 1997;13:29–37.Google Scholar
  43. 43.
    Sequeira H, Cabrita J, de Vroey C, Wuytack-Raes C. Contribution to our knowledge of Trichophyton megninii. J Med Vet Mycol. 1991;29:417–8.PubMedCrossRefGoogle Scholar
  44. 44.
    Ohst T, de Hoog GS, Presber W, Gräser Y. Origins of microsatellite diversity in the Trichophyton rubrumT. violaceum clade (dermatophytes). J Clin Microbiol. 2004;42:4444–48.PubMedCrossRefGoogle Scholar
  45. 45.
    Kane J, Krajden S, Summerbell RC, Sibbald RG. Infections caused by Trichophyton raubitschekii: clinical and epidemiological features. Mycoses. 1990;33:499–506.PubMedGoogle Scholar
  46. 46.
    Tietz HJ, Hopp M, Gräser Y. First isolation of Trichophyton raubitschekii (syn. T. rubrum) in Europe. Mycoses. 2002;45:10–4.PubMedCrossRefGoogle Scholar
  47. 47.
    Brasch J, Gräser Y. The raubitschekii variant of Trichophyton rubrum has reached Germany. Hautarzt. 2005;56:473–7.PubMedCrossRefGoogle Scholar
  48. 48.
    Summerbell RC. Trichophyton, Microsporum, Epidermophyton, and agents of superficial mycosis. In: Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH, editors. Manual of clinical microbiology. 9th ed. Washington DC: ASM Press (in press).Google Scholar
  49. 49.
    Sharma R, de Hoog GS, Presber W, Gräser Y. A virulent genotype of Microsporum canis is responsible for the majority of human infections. J Med Microbiol. 2007;56:1377–85.PubMedCrossRefGoogle Scholar
  50. 50.
    Brasch J, Gräser Y. Trichophyton eboreum sp. nov. isolated from human skin. J Clin Microbiol. 2005;43:5230–7.PubMedCrossRefGoogle Scholar
  51. 51.
    Sharma R, Rajak RC, Pandey AK, Gräser Y. Internal Transcribed Spacer (ITS) of rDNA of appendaged and non-appendaged strains of Microsporum gypseum reveals Microsporum appendiculatum as its synonym. Antonie Van Leeuwenhoek. 2006;20:197–202.CrossRefGoogle Scholar
  52. 52.
    Avise JC, Ball RM. Principles of genealogical concordance in species concepts and biological taxonomy. Oxford Surv Evol Biol. 1990;7:45–67.Google Scholar
  53. 53.
    Maiden MCJ, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou JJ, Zurth K, Caugant DA, et al. Multilocus sequence typing—a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA. 1998;95:3140–5.PubMedCrossRefGoogle Scholar
  54. 54.
    Jackson CJ, Barton RC, Evans EG. Species identification and strain differentiation of dermatophyte fungi by analysis of ribosomal-DNA intergenic spacer regions. J Clin Microbiol. 1999;37:931–6.PubMedGoogle Scholar
  55. 55.
    Henderson ST, Petes TD. Instability of simple sequence DNA in Saccharomyces cerevisiae. Mol Cell Biol. 1992;12:2749–57.PubMedGoogle Scholar
  56. 56.
    Gräser Y, El Fari M, Sterry W, Presber W, Tietz HJ. Identification of common dermatophytes (Trichophyton, Microsporum, Epidermophyton) using PCR fingerprinting. Br J Dermatol. 1998;138:576–82.PubMedCrossRefGoogle Scholar
  57. 57.
    Liu D, Coloe S, Baird R, Pedersen J. Application of PCR to the identification of dermatophyte fungi. J Med Microbiol. 2000;49:493–7.PubMedGoogle Scholar
  58. 58.
    Currah RS. Taxonomy of the Onygenales: Arthrodermataceae, Gymnoascaceae, Myccotrichaceae and Onygenaceae. Mycotaxon. 1985;24:1–216.Google Scholar
  59. 59.
    Leclerc MC, Philippe H, Guého E. Phylogeny of dermatophytes and dimorphic fungi based on large subunit ribosomal RNA sequence comparisons. J Med Vet Mycol. 1994;32:331–41.PubMedCrossRefGoogle Scholar
  60. 60.
    Harmsen D, Schwinn A, Weig M, Brocker EB, Heesemann J. Phylogeny and dating of some pathogenic keratinophilic fungi using small subunit ribosomal RNA. J Med Vet Mycol. 1995;33:299–303.PubMedCrossRefGoogle Scholar
  61. 61.
    Hirai A, Kano R, Nakamura Y, Watanabe S, Hasegawa A. Molecular taxonomy of dermatophytes and related fungi by chitin synthase 1 (CHS1) gene sequences. Antonie Van Leeuwenhoek. 2003;83:11–20.PubMedCrossRefGoogle Scholar
  62. 62.
    Campbell CK, Borman AM, Linton CJ, Bridge PD, Johnson EM. Arthroderma olidum, sp. nov. A new addition to the Trichophyton terrestre complex. Med Mycol. 2006;44:451–9.PubMedCrossRefGoogle Scholar
  63. 63.
    Kawasaki M, Aoki M, Ishizaki H. Phylogenetic relationships of some Microsporum and Arthroderma species inferred from mitochondrial DNA analysis. Mycopathologia. 1995;130:11–21.PubMedCrossRefGoogle Scholar
  64. 64.
    Okeke CN, Tsuboi R, Kawai M, Hiruma M, Ogawa H. Isolation of an intron-containing partial sequence of the gene encoding dermatophyte actin (ACT) and detection of a fragment of the transcript by reverse transcription-nested PCR as a means of assessing the viability of dermatophytes in skin scales. J Clin Microbiol. 2001;39:101–6.PubMedCrossRefGoogle Scholar
  65. 65.
    Kanbe T, Suzuki Y, Kamiya A, Mochizuki T, Fujihiro M, Kikuchi A. PCR-based identification of common dermatophyte species using primer sets specific for the DNA topoisomerase II genes. J Dermatol Sci. 2003;32:151–61.PubMedCrossRefGoogle Scholar
  66. 66.
    Kanbe T, Suzuki Y, Kamiya A, Mochizuki T, Kawasaki M, Fujihiro M, Kikuchi A. Species-identification of dermatophytes Trichophyton, Microsporum and Epidermophyton by PCR and PCR-RFLP targeting of the DNA topoisomerase II genes. J Dermatol Sci. 2003;33:41–54.PubMedCrossRefGoogle Scholar
  67. 67.
    Ninet B, Jan I, Bontems O, Lechenne B, Jousson O, Panizzon R, Lew D, Monod M. Identification of dermatophyte species by 28S ribosomal DNA sequencing with a commercial kit. J Clin Microbiol. 2003;41:826–30.PubMedCrossRefGoogle Scholar
  68. 68.
    Trotha R, Gräser Y, Platt J, Koster A, König B, König W, Freytag C. Tinea barbae caused by a zoophilic strain of Trichophyton interdigitale. Mycoses. 2003;46:60–3.PubMedCrossRefGoogle Scholar
  69. 69.
    Hironaga M, Fujigaki T, Watanabe S. Trichophyton mentagrophytes skin infections in laboratory animals as a cause of zoonosis. Mycopathologia. 1981;73:101–4.PubMedCrossRefGoogle Scholar
  70. 70.
    Makimura K, Mochizuki T, Hasegawa A, Uchida K, Saito H, Yamaguchi H. Phylogenetic classification of Trichophyton mentagrophytes complex strains based on DNA sequences of nuclear ribosomal internal transcribed spacer 1 regions. J Clin Microbiol. 1998;36:2629–33.PubMedGoogle Scholar
  71. 71.
    Takashio M. Une nouvelle forme sexuée du complexe Trichophyton mentagrophytes, Arthroderma vanbreuseghemii sp. nov. Ann Parasitol (Paris). 1975;48:713–32.Google Scholar
  72. 72.
    Hata Y, Amagai M, Naka W, Harada R, Nishkawa T. Two cases of Trichophyton mentagrophytes infection contracted from a hamster and a chinchilla. Jpn J Med Mycol. 2000;41:269–73.Google Scholar
  73. 73.
    Kim JA, Takahashi Y, Tanaka R, Fukushima K, Nishimura K, Miyaji M. Identification and subtyping of Trichophyton mentagrophytes by random amplified polymorphic DNA. Mycoses. 2001;44:157–65.PubMedCrossRefGoogle Scholar
  74. 74.
    Symoens F, Willenz P, Rouma V, Planard C, Nolard N. Isoelectric focusing applied to taxonomic differentiation of the Trichophyton mentagrophytes complex and the related Trichophyton interdigitale. Mycoses. 1989;32:652–63.PubMedGoogle Scholar
  75. 75.
    Ranganathan S, Balajee SAM, Menon T. Mating patterns of dermatophytes of diverse origin in India. Mycopathologia. 1996;136:91–4.PubMedCrossRefGoogle Scholar
  76. 76.
    Fumeaux J, Mock M, Ninet B, Jan I, Bontems O, Lechenne B, Lew D, Panizzon RG, Jousson O, Monod M. First report of Arthroderma benhamiae in Switzerland. Dermatology. 2004;208:244–50.PubMedCrossRefGoogle Scholar
  77. 77.
    Nishio K, Kawasaki M, Ishizaki H. Phylogeny of the genera Trichophyton using mitochondrial DNA analysis. Mycopathologia. 1992;117:127–32.PubMedCrossRefGoogle Scholar
  78. 78.
    Deng S, Bulmer GS, Summerbell RC, de Hoog GS, Hui Y, Gräser Y. Changes in frequency of agents of tinea capitis in school children from Western China suggest slow migration rates in dermatophytes. Med Mycol. 2008 (in press).Google Scholar
  79. 79.
    Ivanova LG, Polyakov ID. Trichophyton sarkisovii Ivanova & Polyakov, sp. nov. – a new species of pathogenic fungus giving rise to dermatomycosis of camel. Mikol Fitopatol. 1983;17:363–7.Google Scholar
  80. 80.
    Takahashi Y, Sano A, Takizawa K, Fukushima K, Miyaji M, Nishimura K. The epidemiology and mating behaviour of Arthroderma benhamiae var. erinacei in household four-toed hedgehogs (Atelerix albiventris) in Japan. Nippon Ishinkin Gakkai Zasshi. 2003;44:31–8.PubMedGoogle Scholar
  81. 81.
    Scott DB. An outbreak of ringworm in karakul sheep caused by a physiological variant of Trichophyton verrucosum Bodin. Onderstepoort J Vet Res. 1975;42:49–52.PubMedGoogle Scholar
  82. 82.
    Gräser Y, Kuijpers AFA, Presber W, de Hoog GS. Molecular taxonomy of the Trichophyton rubrum complex. J Clin Microbiol. 2000;38:3329–36.PubMedGoogle Scholar
  83. 83.
    Jackson CJ, Barton RC, Kelly SL, Evans EG. Strain identification of Trichophyton rubrum by specific amplification of subrepeat elements in the ribosomal DNA nontranscribed spacer. J Clin Microbiol. 2000;38:4527–34.PubMedGoogle Scholar
  84. 84.
    Gupta AK, Kohli Y, Summerbell RC. Exploratory study of single-copy genes and ribosomal intergenic spacers for distinction of dermatophytes. Stud Mycol. 2002;47:87–96.Google Scholar
  85. 85.
    Kano R, Okabayashi K, Nakamura Y, Ooka S, Kashima M, Mizoguchi M, Watanabe S, Hasegawa A. Differences among chitin synthase I gene sequences in Trichophyton rubrum and T. violaceum. Med Mycol. 2000;38:47–50.PubMedCrossRefGoogle Scholar
  86. 86.
    Summerbell RC, Cooper E, Bunn U, Jamieson F, Gupta AK. Onychomycosis: a critical study of techniques and criteria for confirming the etiologic significance of nondermatophytes. Med Mycol. 2005;43:39–59.PubMedCrossRefGoogle Scholar
  87. 87.
    Kardjeva V, Summerbell R, Kantardjiev T, Devliotou-Panagiotidou D, Sotiriou E, Gräser Y. Rapid diagnosis of onychomycosis with subtyping of Trichophyton rubrum strains. J Clin Microbiol. 2006;44:1419–27.PubMedCrossRefGoogle Scholar
  88. 88.
    Iwen PC. Molecular detection and typing of fungal pathogens. Clin Lab Med. 2003;23:781–99.PubMedCrossRefGoogle Scholar
  89. 89.
    Beifuß B, Bezold G, Korting, HC. Etablierung einer molekularen Sofortdiagnostik von fünf gängigen Dermatophyten-Spezies aus nativem Patientenmaterial mittels einer sensitiven PCR-ELISA-Methode innerhalb von 24 Stunden: 40. Congress of „Deutschsprachige Mykologische Gesellschaft (DMYKG)“, September 2006, Innsbruck.Google Scholar
  90. 90.
    Savin C, Huck S, Rolland C, Benderdouche M, Faure O, Noacco G, Menotti J, Candolfi E, Pelloux H, Grillot R, Coupe S, Derouin F. Multicenter evaluation of a commercial PCR-enzyme-linked immunosorbent assay diagnostic kit (Onychodiag) for diagnosis of dermatophytic onychomycosis. J Clin Microbiol. 2007;45:1205–10.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Yvonne Gräser
    • 1
  • James Scott
    • 2
    • 3
  • Richard Summerbell
    • 3
  1. 1.Department of Parasitology, Institute of Microbiology and HygieneCharité, Humboldt UniversityBerlinGermany
  2. 2.Department of Public Health SciencesUniversity of TorontoTorontoCanada
  3. 3.Sporometrics Inc.TorontoCanada

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