{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T11:14:25Z","timestamp":1783509265518,"version":"3.55.0"},"reference-count":29,"publisher":"MDPI AG","issue":"6","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,11]]},"abstract":"\n Background<\/jats:title>\n \n Onychomycosis is estimated to occur in approximately 10% of the global population, with most cases caused by\n Trichophyton rubrum<\/jats:italic>\n . Some persistent onychomycosis is caused by mixed infections of\n T rubrum<\/jats:italic>\n and one or more co-infecting nondermatophyte molds (NDMs). In onychomycosis,\n T rubrum<\/jats:italic>\n strain types may naturally switch and may also be triggered to switch in response to antifungal therapy.\n T rubrum<\/jats:italic>\n strain types in mixed infections of onychomycosis have not been characterized.\n <\/jats:p>\n <\/jats:sec>\n \n Methods<\/jats:title>\n \n T rubrum<\/jats:italic>\n DNA strains in mixed infections of onychomycosis containing co-infecting NDMs were compared with a baseline North American population through polymerase chain reaction amplification of ribosomal DNA tandemly repetitive subelements (TRSs) 1 and 2. The baseline DNA strain types were determined from 102 clinical isolates of\n T rubrum<\/jats:italic>\n . The\n T rubrum<\/jats:italic>\n DNA strain types from mixed infections were determined from 63 repeated toenail samples from 15 patients.\n <\/jats:p>\n <\/jats:sec>\n \n Results<\/jats:title>\n \n Two unique TRS-2 types among the clinical isolates contributed to four unique TRS-1 and TRS-2 strain types. Six TRS-1 and TRS-2 strain types represented 92% of the clinical isolates of\n T rubrum<\/jats:italic>\n . Four TRS-1 and TRS-2 strain types accounted for 100% of the\n T rubrum<\/jats:italic>\n within mixed infections.\n <\/jats:p>\n <\/jats:sec>\n \n Conclusions<\/jats:title>\n \n Four unique North American\n T rubrum<\/jats:italic>\n strains were identified. In support of a shared ancestry, the\n T rubrum<\/jats:italic>\n DNA strain types found in mixed infections with NDMs were among the most abundant types. A population of\n T rubrum<\/jats:italic>\n strains in mixed infections of onychomycosis has been characterized, with more than one strain detected in some nails. The presence of a co-infecting NDM in mixed infections may contribute to failed therapy by stabilizing the\n T rubrum<\/jats:italic>\n strain type, possibly preventing the antifungal therapy\u2013induced strain type switching observed with infections caused by\n T rubrum<\/jats:italic>\n alone.\n <\/jats:p>\n <\/jats:sec>","DOI":"10.7547\/17-201","type":"journal-article","created":{"date-parts":[[2020,8,18]],"date-time":"2020-08-18T15:32:24Z","timestamp":1597764744000},"source":"Crossref","is-referenced-by-count":4,"title":["Trichophyton rubrum DNA Strains in Patients with Onychomycosis with Persistent Mixed Infections Involving a Nondermatophyte Mold"],"prefix":"10.3390","volume":"110","author":[{"given":"Aditya K.","family":"Gupta","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kerry-Ann","family":"Nakrieko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","reference":[{"key":"i8750-7315-110-6-Article_3-b01","series-title":"J Clin Pharm Ther","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1111\/j.1365-2710.2009.01107.x","article-title":"Toenail onychomycosis: an important global disease burden","volume":"35","author":"Thomas","year":"2010","unstructured":"Thomas\n J\n \n \n Jacobson\n GA\n \n \n Narkowicz\n CK\n \n :\n\t\t\t\t\t\n Toenail onychomycosis: an important global disease burden.\n\t\t\t\t\tJ Clin Pharm Ther35: 497,\n\t\t\t\t\t2010.\n\t\t\t\t10.1111\/j.1365-2710.2009.01107.x20831675"},{"key":"i8750-7315-110-6-Article_3-b02","series-title":"J Eur Acad Dermatol Venereol","doi-asserted-by":"publisher","first-page":"1567","DOI":"10.1111\/jdv.13677","article-title":"The prevalence of unsuspected onychomycosis and its causative organisms in a multicentre Canadian sample of 30 000 patients visiting physicians' offices","volume":"30","author":"Gupta","year":"2016","unstructured":"Gupta\n AK\n \n \n Gupta\n G\n \n \n Jain\n HC\n \n :\n\t\t\t\t\t\n The prevalence of unsuspected onychomycosis and its causative organisms in a multicentre Canadian sample of 30 000 patients visiting physicians' offices.\n\t\t\t\t\tJ Eur Acad Dermatol Venereol30: 1567,\n\t\t\t\t\t2016.\n\t\t\t\t10.1111\/jdv.13677"},{"key":"i8750-7315-110-6-Article_3-b03","series-title":"Med Mycol","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1080\/13693780410001712043","article-title":"Onychomycosis: a critical study of techniques and criteria for confirming the etiologic significance of nondermatophytes","volume":"43","author":"Summerbell","year":"2005","unstructured":"Summerbell\n RC:\n \n \n Onychomycosis: a critical study of techniques and criteria for confirming the etiologic significance of nondermatophytes.\n\t\t\t\t\tMed Mycol43: 39,\n\t\t\t\t\t2005.\n\t\t\t\t1571260710.1080\/13693780410001712043"},{"key":"i8750-7315-110-6-Article_3-b04","series-title":"J Am Acad Dermatol","doi-asserted-by":"publisher","first-page":"494","DOI":"10.1016\/j.jaad.2011.02.038","article-title":"Systematic review of nondermatophyte mold onychomycosis: diagnosis, clinical types, epidemiology, and treatment","volume":"66","author":"Gupta","year":"2012","unstructured":"Gupta\n AK\n \n \n Drummond-Main\n C\n \n \n Cooper\n EA\n \n :\n\t\t\t\t\t\n Systematic review of nondermatophyte mold onychomycosis: diagnosis, clinical types, epidemiology, and treatment.\n\t\t\t\t\tJ Am Acad Dermatol66: 494,\n\t\t\t\t\t2012.\n\t\t\t\t10.1016\/j.jaad.2011.02.03821820203"},{"key":"i8750-7315-110-6-Article_3-b05","series-title":"Mycoses","doi-asserted-by":"publisher","first-page":"558","DOI":"10.1111\/myc.12504","article-title":"Non-dermatophytic onychomycosis diagnostic criteria: an unresolved question","volume":"59","author":"Bombace","year":"2016","unstructured":"Bombace\n F\n \n \n Iovene\n MR\n \n \n Galdiero\n M\n \n :\n\t\t\t\t\t\n Non-dermatophytic onychomycosis diagnostic criteria: an unresolved question.\n\t\t\t\t\tMycoses59: 558,\n\t\t\t\t\t2016.\n\t\t\t\t10.1111\/myc.1250427061613"},{"key":"i8750-7315-110-6-Article_3-b06","series-title":"JAPMA","first-page":"280","article-title":"Onychomycosis infections: do polymerase chain reaction and culture reports agree?","volume":"107","author":"Gupta","year":"2017","unstructured":"Gupta\n AK\n \n \n Nakrieko\n K-A:\n \n \n Onychomycosis infections: do polymerase chain reaction and culture reports agree?\n JAPMA\n 107\n : \n 280,\n\t\t\t\t\t2017."},{"key":"i8750-7315-110-6-Article_3-b07","series-title":"Br J Dermatol","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1111\/j.1365-2133.2008.08805.x","article-title":"New criteria for the laboratory diagnosis of nondermatophyte moulds in onychomycosis","volume":"160","author":"Shemer","year":"2009","unstructured":"Shemer\n A\n \n \n Davidovici\n B\n \n \n Grunwald\n MH\n \n :\n\t\t\t\t\t\n New criteria for the laboratory diagnosis of nondermatophyte moulds in onychomycosis.\n\t\t\t\t\tBr J Dermatol160: 37,\n\t\t\t\t\t2009.\n\t\t\t\t10.1111\/j.1365-2133.2008.08805.x18764841"},{"key":"i8750-7315-110-6-Article_3-b08","series-title":"J Clin Microbiol","doi-asserted-by":"publisher","first-page":"931","DOI":"10.1128\/JCM.37.4.931-936.1999","article-title":"Species identification and strain differentiation of dermatophyte fungi by analysis of ribosomal-DNA intergenic spacer regions","volume":"37","author":"Jackson","year":"1999","unstructured":"Jackson\n CJ\n \n \n Barton\n RC\n \n \n Evans\n EG:\n \n \n Species identification and strain differentiation of dermatophyte fungi by analysis of ribosomal-DNA intergenic spacer regions.\n\t\t\t\t\tJ Clin Microbiol37: 931,\n\t\t\t\t\t1999.\n\t\t\t\t1007450410.1128\/JCM.37.4.931-936.1999"},{"key":"i8750-7315-110-6-Article_3-b09","series-title":"J Clin Microbiol","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1128\/JCM.39.2.685-690.2001","article-title":"Rapid discrimination among dermatophytes, Scytalidium spp., and other fungi with a PCR-restriction fragment length polymorphism ribotyping method","volume":"39","author":"Machouart-Dubach","year":"2001","unstructured":"Machouart-Dubach\n M\n \n \n Lacroix\n C\n \n \n de Chauvin\n MF\n \n :\n\t\t\t\t\t\n Rapid discrimination among dermatophytes, Scytalidium spp., and other fungi with a PCR-restriction fragment length polymorphism ribotyping method.\n\t\t\t\t\tJ Clin Microbiol39: 685,\n\t\t\t\t\t2001.\n\t\t\t\t1115812810.1128\/JCM.39.2.685-690.2001"},{"key":"i8750-7315-110-6-Article_3-b10","series-title":"Br J Dermatol","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1111\/j.1365-2133.2009.09291.x","article-title":"Evaluation of a polymerase chain reaction-restriction fragment length polymorphism assay for dermatophyte and nondermatophyte identification in onychomycosis","volume":"161","author":"Bontems","year":"2009","unstructured":"Bontems\n O\n \n \n Hauser\n PM\n \n \n Monod\n M:\n \n \n Evaluation of a polymerase chain reaction-restriction fragment length polymorphism assay for dermatophyte and nondermatophyte identification in onychomycosis.\n\t\t\t\t\tBr J Dermatol161: 791,\n\t\t\t\t\t2009.\n\t\t\t\t10.1111\/j.1365-2133.2009.09291.x19558597"},{"key":"i8750-7315-110-6-Article_3-b11","series-title":"Br J Dermatol","doi-asserted-by":"publisher","first-page":"1038","DOI":"10.1111\/j.1365-2133.2009.09249.x","article-title":"Molecular detection of dermatophytes and nondermatophytes in onychomycosis by nested polymerase chain reaction based on 28S ribosomal RNA gene sequences","volume":"161","author":"Ebihara","year":"2009","unstructured":"Ebihara\n M\n \n \n Makimura\n K\n \n \n Sato\n K\n \n :\n\t\t\t\t\t\n Molecular detection of dermatophytes and nondermatophytes in onychomycosis by nested polymerase chain reaction based on 28S ribosomal RNA gene sequences.\n\t\t\t\t\tBr J Dermatol161: 1038,\n\t\t\t\t\t2009.\n\t\t\t\t10.1111\/j.1365-2133.2009.09249.x19566663"},{"key":"i8750-7315-110-6-Article_3-b12","series-title":"Mycopathologia","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1007\/s11046-008-9108-1","article-title":"Strain differentiation of dermatophytes","volume":"166","author":"Abdel-Rahman","year":"2008","unstructured":"Abdel-Rahman\n SM:\n \n \n Strain differentiation of dermatophytes.\n\t\t\t\t\tMycopathologia166: 319,\n\t\t\t\t\t2008.\n\t\t\t\t10.1007\/s11046-008-9108-118478358"},{"key":"i8750-7315-110-6-Article_3-b13","series-title":"J Clin Microbiol","doi-asserted-by":"publisher","first-page":"1419","DOI":"10.1128\/JCM.44.4.1419-1427.2006","article-title":"Forty-eight-hour diagnosis of onychomycosis with subtyping of Trichophyton rubrum strains","volume":"44","author":"Kardjeva","year":"2006","unstructured":"Kardjeva\n V\n \n \n Summerbell\n R\n \n \n Kantardjiev\n T\n \n :\n\t\t\t\t\t\n Forty-eight-hour diagnosis of onychomycosis with subtyping of Trichophyton rubrum strains.\n\t\t\t\t\tJ Clin Microbiol44: 1419,\n\t\t\t\t\t2006.\n\t\t\t\t1659787110.1128\/JCM.44.4.1419-1427.2006"},{"key":"i8750-7315-110-6-Article_3-b14","series-title":"J Clin Microbiol","doi-asserted-by":"publisher","first-page":"4527","DOI":"10.1128\/JCM.38.12.4527-4534.2000","article-title":"Strain identification of Trichophyton rubrum by specific amplification of subrepeat elements in the ribosomal DNA nontranscribed spacer","volume":"38","author":"Jackson","year":"2000","unstructured":"Jackson\n CJ\n \n \n Barton\n RC\n \n \n Kelly\n SL\n \n :\n\t\t\t\t\t\n Strain identification of Trichophyton rubrum by specific amplification of subrepeat elements in the ribosomal DNA nontranscribed spacer.\n\t\t\t\t\tJ Clin Microbiol38: 4527,\n\t\t\t\t\t2000.\n\t\t\t\t10.1128\/JCM.38.12.4527-4534.200011101591"},{"key":"i8750-7315-110-6-Article_3-b15","series-title":"J Med Microbiol","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1099\/jmm.0.46236-0","article-title":"Strain differentiation of Trichophyton rubrum by randomly amplified polymorphic DNA and analysis of rDNA nontranscribed spacer","volume":"55","author":"Baeza","year":"2006","unstructured":"Baeza\n LC\n \n \n Matsumoto\n MT\n \n \n Almeida\n AMF\n \n :\n\t\t\t\t\t\n Strain differentiation of Trichophyton rubrum by randomly amplified polymorphic DNA and analysis of rDNA nontranscribed spacer.\n\t\t\t\t\tJ Med Microbiol55: 429,\n\t\t\t\t\t2006.\n\t\t\t\t1653399110.1099\/jmm.0.46236-0"},{"key":"i8750-7315-110-6-Article_3-b16","series-title":"J Med Microbiol","doi-asserted-by":"publisher","first-page":"1058","DOI":"10.1099\/jmm.0.47138-0","article-title":"Microsatellite markers reveal geographic population differentiation in Trichophyton rubrum","volume":"56","author":"Gr\u00e4ser","year":"2007","unstructured":"Gr\u00e4ser\n Y\n \n \n Fr\u00f6hlich\n J\n \n \n Presber\n W\n \n :\n\t\t\t\t\t\n Microsatellite markers reveal geographic population differentiation in Trichophyton rubrum.\n\t\t\t\t\tJ Med Microbiol56: 1058,\n\t\t\t\t\t2007.\n\t\t\t\t1764471310.1099\/jmm.0.47138-0"},{"key":"i8750-7315-110-6-Article_3-b17","series-title":"Mycoses","doi-asserted-by":"publisher","first-page":"348","DOI":"10.1111\/myc.12602","article-title":"Identification and molecular epidemiology of dermatophyte isolates by repetitive-sequence-PCR-based DNA fingerprinting using the DiversiLab system in Turkey","volume":"60","author":"Koc","year":"2017","unstructured":"Koc\n AN\n \n \n Atalay\n MA\n \n \n Inci\n M\n \n :\n\t\t\t\t\t\n Identification and molecular epidemiology of dermatophyte isolates by repetitive-sequence-PCR-based DNA fingerprinting using the DiversiLab system in Turkey.\n\t\t\t\t\tMycoses60: 348,\n\t\t\t\t\t2017.\n\t\t\t\t10.1111\/myc.1260228220547"},{"key":"i8750-7315-110-6-Article_3-b18","series-title":"JAPMA","first-page":"330","article-title":"Molecular determination of mixed infections of dermatophytes and nondermatophyte moulds in individuals with onychomycosis","volume":"104","author":"Gupta","year":"2014","unstructured":"Gupta\n A\n \n \n Nakrieko\n K-A:\n \n \n Molecular determination of mixed infections of dermatophytes and nondermatophyte moulds in individuals with onychomycosis.\n\t\t\t\t\tJAPMA104: 330,\n\t\t\t\t\t2014."},{"key":"i8750-7315-110-6-Article_3-b19","series-title":"Br J Dermatol","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1111\/bjd.13165","article-title":"Trichophyton rubrum DNA strain switching increases in patients with onychomycosis failing antifungal treatments","volume":"172","author":"Gupta","year":"2015","unstructured":"Gupta\n AK\n \n \n Nakrieko\n K-A:\n \n \n \n Trichophyton rubrum DNA strain switching increases in patients with onychomycosis failing antifungal treatments.\n\t\t\t\t\tBr J Dermatol172: 74,\n\t\t\t\t\t2015.\n\t\t\t\t2490345110.1111\/bjd.13165"},{"key":"i8750-7315-110-6-Article_3-b20","series-title":"Clin Microbiol Rev","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1128\/CMR.12.1.126","article-title":"The evolutionary biology and population genetics underlying fungal strain typing","volume":"12","author":"Taylor","year":"1999","unstructured":"Taylor\n JW\n \n \n Geiser\n DM\n \n \n Burt\n A\n \n :\n\t\t\t\t\t\n The evolutionary biology and population genetics underlying fungal strain 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fungi.\n\t\t\t\t\tMed Mycol44: 199,\n\t\t\t\t\t2006.\n\t\t\t\t10.1080\/1369378060060681016702098"},{"key":"i8750-7315-110-6-Article_3-b23","series-title":"J Clin Microbiol","doi-asserted-by":"publisher","first-page":"4444","DOI":"10.1128\/JCM.42.10.4444-4448.2004","article-title":"Origins of microsatellite diversity in the Trichophyton rubrum-T. violaceum clade (dermatophytes)","volume":"42","author":"Ohst","year":"2004","unstructured":"Ohst\n T\n \n \n De Hoog\n S\n \n \n Presber\n W\n \n :\n\t\t\t\t\t\n Origins of microsatellite diversity in the Trichophyton rubrum-T. violaceum clade (dermatophytes).\n\t\t\t\t\tJ Clin Microbiol42: 4444,\n\t\t\t\t\t2004.\n\t\t\t\t1547229110.1128\/JCM.42.10.4444-4448.2004"},{"key":"i8750-7315-110-6-Article_3-b24","series-title":"Mycoses","doi-asserted-by":"publisher","first-page":"726","DOI":"10.1111\/j.1439-0507.2010.02007.x","article-title":"Molecular typing of Trichophyton rubrum clinical isolates from Poland","volume":"54","author":"Hryncewicz-Gw\u00f3\u017ad\u017a","year":"2011","unstructured":"Hryncewicz-Gw\u00f3\u017ad\u017a\n A\n \n \n Jagielski\n T\n \n \n Sadakierska-Chudy\n A\n \n :\n\t\t\t\t\t\n Molecular typing of Trichophyton rubrum clinical isolates from Poland.\n\t\t\t\t\tMycoses54: 726,\n\t\t\t\t\t2011.\n\t\t\t\t10.1111\/j.1439-0507.2010.02007.x"},{"key":"i8750-7315-110-6-Article_3-b25","series-title":"Br J Dermatol","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1046\/j.1365-2133.2003.05060.x","article-title":"Molecular strain typing of Trichophyton rubrum indicates multiple strain involvement in onychomycosis","volume":"148","author":"Yazdanparast","year":"2003","unstructured":"Yazdanparast\n A\n \n \n Jackson\n CJ\n \n \n Barton\n RC\n \n :\n\t\t\t\t\t\n Molecular strain typing of Trichophyton rubrum indicates multiple strain involvement in onychomycosis.\n\t\t\t\t\tBr J Dermatol148: 51,\n\t\t\t\t\t2003.\n\t\t\t\t1253459410.1046\/j.1365-2133.2003.05060.x"},{"key":"i8750-7315-110-6-Article_3-b26","series-title":"Cutis","first-page":"237","article-title":"Molecular analysis of dermatophytes suggests spread of infection among household members","volume":"91","author":"Ghannoum","year":"2013","unstructured":"Ghannoum\n MA\n \n \n Mukherjee\n PK\n \n \n Warshaw\n EM\n \n :\n\t\t\t\t\t\n Molecular analysis of dermatophytes suggests spread of infection among household members.\n\t\t\t\t\tCutis91: 237,\n\t\t\t\t\t2013.\n\t\t\t\t23772429"},{"key":"i8750-7315-110-6-Article_3-b27","series-title":"J Clin Microbiol","doi-asserted-by":"publisher","first-page":"767","DOI":"10.1128\/jcm.34.4.767-777.1996","article-title":"Most frequent scenario for recurrent Candida vaginitis is strain maintenance with \u201csubstrain shuffling\u201d: demonstration by sequential DNA fingerprinting with probes Ca3, C1, and CARE2","volume":"34","author":"Lockhart","year":"1996","unstructured":"Lockhart\n SR\n \n \n Reed\n BD\n \n \n Pierson\n CL\n \n :\n\t\t\t\t\t\n Most frequent scenario for recurrent Candida vaginitis is strain maintenance with \u201csubstrain shuffling\u201d: demonstration by sequential DNA fingerprinting with probes Ca3, C1, and CARE2.\n\t\t\t\t\tJ Clin Microbiol34: 767,\n\t\t\t\t\t1996.\n\t\t\t\t881508210.1128\/jcm.34.4.767-777.1996"},{"key":"i8750-7315-110-6-Article_3-b28","series-title":"Nature","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1038\/284426a0","article-title":"Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae","volume":"284","author":"Szostak","year":"1980","unstructured":"Szostak\n JW\n \n \n Wu\n R:\n \n \n Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae.\n\t\t\t\t\tNature284: 426,\n\t\t\t\t\t1980.\n\t\t\t\t10.1038\/284426a06987539"},{"key":"i8750-7315-110-6-Article_3-b29","series-title":"J Am Acad Dermatol","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1067\/mjd.2002.119674","article-title":"Reactivity to trichophytin antigen in patients with onychomycosis: effect of terbinafine","volume":"46","author":"Elewski","year":"2002","unstructured":"Elewski\n BE\n \n \n El Charif\n M\n \n \n Cooper\n KD\n \n :\n\t\t\t\t\t\n Reactivity to trichophytin antigen in patients with onychomycosis: effect of terbinafine.\n\t\t\t\t\tJ Am Acad Dermatol46: 371,\n\t\t\t\t\t2002.\n\t\t\t\t10.1067\/mjd.2002.11967411862171"}],"container-title":["Journal of the American Podiatric Medical 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