Mycopathologia (2015) 179:159–161 DOI 10.1007/s11046-014-9823-8
A Chronic Disseminated Dermatophytosis Due to Trichophyton violaceum Ping Zhan • Zhi-hua Li • Chengfang Geng • Qing Jiang • Yun Jin • Somayeh Dolatabadi Weida Liu • G. Sybren de Hoog
•
Received: 13 April 2014 / Accepted: 1 October 2014 / Published online: 17 October 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract A 48-year-old female had presented dandruff and breakable hair for more than 40 years, dry scaly erythema on bilateral palms and feet accompanying with nail destruction for 20 years, and scaling papules on the buttock for 5 years. Direct microscopic examination showed endothrix anthroconidia within broken hair and septate and branched hyphae within skin and nail lesion. Fungal cultures from all infected sites were examined by morphology, ITS sequencing, and random amplified polymorphic DNA fingerprinting, and were identified as Trichophyton violaceum from the same source. The patient was treated with oral terbinafine 0.25 g/day as well as with 1 % terbinafine gel for external use and with 2 % ketoconazole lotion for shampoo and bath. A follow-up after 4 weeks showed that the lesions decreased significantly.
P. Zhan Z. Li C. Geng Q. Jiang Y. Jin Specialized Dermatology Hospital of Jiangxi Province, Nanchang, China P. Zhan W. Liu (&) Department of Mycology, Institute of Dermatology, Chinese Academy of Medical Science and Peking Union Medical College, No. 12 Jiang Wangmiao Street, Nanjing 210042, China e-mail: [email protected] S. Dolatabadi G. S. de Hoog CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands
Keywords Trichophyton violaceum Dermatophytosis Fingerprinting
Introduction Trichophyton violaceum is a common superficial fungus endemic in parts of America, Africa, Europe, and Asia [1–5]. In China, the species is one of the preponderant agents of tinea capitis, mainly being isolated in local regions of Southern and Northwestern China [4, 5]. Other infections caused by T. violaceum, such as tinea corporis, tinea pedis, tinea manuum, and onychomycosis, are infrequently reported [1, 3]. Here, we report a case of disseminated dermatophytosis by T. violaceum which started as tinea capitis 40 years ago and gradually extended to other parts of the body presenting as tinea cruris, tinea pedis, and tinea manus, as well as onychomycosis. Strains from different infected sites were confirmed to be T. violaceum by phenotypic and molecular data, while molecular fingerprinting with random amplified polymorphic DNA (RAPD) confirmed that all isolated strains came from the same source.
Case Report A 48-year-old female from Xinjian area, located nearby Nanchang city, Jiangxi province, South China,
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was admitted to our dermatology clinic with a history of disseminated skin lesions for about 5 years. She had been working as a farmer and was engaged in agricultural production for all her life. As a child 40 years ago, she developed dandruff and fragile hairs with scalp pruritus, which could be relieved mildly by Head & Shoulders shampoo but relapsed quickly. About 20 years ago, her palms and soles began to have a problem of dryness, desquamation, and skin fissures. At the same time, her fingernails and toenails became rough, hyperkeratotic, and crumbled with yellowish to brown discoloration. Five years before admission, her buttocks presented with erythema, papules, and desquamation with pruritus. The lesions had aggravated particularly during the past 2 years. Patient was cachectic but had never sought medical care up to now and denied significant medical problems. The infection was not found in other members of the family who used to live close together in a rural setting. Physical examination revealed a small, cachectic patient (41.2 kg, 148 cm). The hair was dry and dull with isolated scaly patches on the scalp. A few black dots of broken hair could be discerned at close observation. Palms and soles presented a dry, rough, finely fissured surface with onycholysis of the nails. Hyperkeratosis was present around all nails. Scaly, dry erythema with some pin-sized papules could also be seen on both buttocks. No obvious abnormality was found by routine blood examination. Direct microscopic examination of broken hairs revealed endothrix of arthroconidia arranged in chains within hair shafts. Wood’s light examination was negative. Direct microscopy of skin and nail specimens also revealed anthroconidia, as well as short, branched, flexuous hyphae. Samples from eight infected sites (hair, left palm, right palm, left sole, right sole, toenail of right foot, fingernail of left hand, buttocks) were inoculated into Sabouraud’s glucose agar containing chloroamphenicol (50 mg/l) with and without cycloheximide (400 mg/l), incubated at 27 °C. After 1 week, similar colonies presented on all agar slants. They were very slow growing, initially glabrous, moist and waxy, later transforming to become heaped and folded, with a deep violet color. To determine the identity of all strains, genomic DNA was extracted using the ZR Fungal/Bacterial DNA MiniPrepTM Kit (Zymo research, USA), and ITS regions were amplified using ITS1 and ITS4 primers. Sequencing results were blasted in database and
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showed 99 % identity to T. violaceum (CBS 374.92), 98 % to T. soundanese (ATCC 24583), and 98 % to Trichophyton rubrum (CBS 376.49). The T. violaceum-specific microsatellite primers T1 [4] were used, and sequencing results showed to be 99 % in accordance with T. violaceum strain IFM 60448. RAPD was implemented subsequently. Four random primers (M13, T3B, (GGA)7, (CAC)5) were applied using recommended protocols by CBS (http://www.isham. org/members/Protocol/index.asp). Bands of all eight strains proved to be completely consistent, strongly suggesting that the pathogens originated from a common source. The final diagnosis was that of a disseminated tinea by a single strain of T. violaceum. Antifungal susceptibility test was performed using the broth microdilution methods (CLSI M38-A2). Both of the minimum effective concentration of caspofungin and micafungin were 0.06 lg/ml. The minimum inhibitory concentration (MIC)100 of voriconazole, itraconazole, terbinafine, and amphotericin B were 0.06, 0.25, 0.03, and 0.25 lg/ml, respectively. And MIC90 of fluconazole was 2 lg/ml. The patient was treated with terbinafine 0.25 g once a day as well as 1 % terbinafine gel for external use and 2 % ketoconazole lotions for shampoo and bath. The second visit after 4 weeks showed a sufficient decrease of the scalp and skin damage, but no improvement of the nails, and after that, the patients was lost to follow-up.
Discussion Dermatophytes usually involve only a single anatomical area, presenting as localized lesions. Chronic and widespread dermatophyte infections are more often associated with onychomycosis and tinea pedis. Disseminated cutaneous dermatophytosis is also commonly seen in patients with impaired acquired cellular immunity or in patients with immunosuppression [6, 7]. The few reported cases of widespread infection in immunocompetent individuals are mainly caused by the anthropophilic dermatophytes T. rubrum and Trichophyton tonsurans [8–10]. These species are frequently carried asymptomatically and may cause infection after autoinoculation [11, 12]. In our case, the patient was an adult woman with a long history of extensive infection for more than 40 years. She declared to be healthy and refused any other medical
Mycopathologia (2015) 179:159–161
examination. Whether she had immunodeficiency remained unknown. Trichophyton violaceum is an anthropophilic dermatophyte which usually causes chronic and inflammatory skin conditions. The infection is mainly localized on scalp region known as tinea black dot. Tinea corporis may follow after dissemination, and this condition is rarely reported [1, 3]. Transmission and expansion of arthropophilic dermatophytes are impacted by inadequate sanitary conditions, disorders of the immune system (steroid or chronic alcohol abuse, diabetes mellitus, pregnancy, and lymphoproliferative disorders), trauma, and age [10–12]. Dessinioti et al. [11] recently reported 34 cases of asymptomatic scalp carriage (ASC) tinea capitis and found there was a statistically significant association of ASC with T. violaceum. In our previous clinical work, we found several cases of adult tinea capitis presented as seborrheic dermatitis, dandruff, dull hair but without broken hair, or obvious inflammation, and the pathogen in all these cases was identified as T. violaceum [5]. We therefore surmise that T. violaceum is specifically associated with ASC and chronic and repeated infections [12].
References 1. Mapelli ET, Colombo L, Crespi E, Menni S. Toenail onychomycosis due to Trichophyton violaceum complex. (An unusual, emerging localization of this anthropophilic dermatophyle). Mycoses. 2012;2:193–4.
161 2. Hogewoning AA, Adegnika AA, Bouwes Bavinck JN et al. Prevalence and causative fungal species of tinea capitis among schoolchildren in Gabon. Mycoses. 2011;5:e354–9. 3. Romano C, Feci L, Fimiani M. Thirty-six cases of epidemic infections due to Trichophyton violaceum in Siena, Italy. Mycoses. 2013. doi:10.1111/myc.12164. 4. Deng S, Bulmer GS, Summerbell RC, De Hoog GS, Hui Y, Gra¨ser Y. Changes in frequency of agents of tinea capitis in school children from Western China suggest slow migration rates in dermatophytes. Med Mycol. 2008;5:421–7. 5. Li Z, Jin Y, Zhan P et al. The clinical characteristics and pathogens of 117 cases of tinea capitis. Chin J Dermatovenerol. 2012;9:808–809, 841 (in chinese). 6. Jime´nez-Puya R, Va´zquez-Bayo C, Rodriguez-Bujaldo´n A, Go´mez Garcı´a F, Moreno-Gime´nez JC. Extensive tinea in a patient with severe combined immunodeficiency. Pediatr Dermatol. 2009;2:213–4. 7. Budihardja D, Freund V, Mayser P. Widespread erosive tinea corporis by Arthroderma benhamiae in a renal transplant recipient: case report. Mycoses. 2010;53(6):530–2. 8. Balci DD, Cetin M. Widespread, chronic, and fluconazoleresistant Trichophyton rubrum infection in an immunocompetent patient. Mycoses. 2008;6:546–8. 9. de Freitas CF, Mulinari-Brenner F, Fontana HR, Gentili AC, Hammerschmidt M. Ichthyosis associated with widespread tinea corporis: report of three cases. An Bras Dermatol. 2013;4:627–30. 10. Calabro` G, Nino M, La Bella S et al. Trichophyton violaceum infection in an adult black patient in Europe. Int J Dermatol. 2011;6:761–3. 11. Dessinioti C, Papadogeorgaki E, Athanasopoulou V, Antoniou C, Stratigos AJ. Screening for asymptomatic scalp carriage in household contacts of patients with tinea capitis during 1997–2011: a retrospective hospital-based study. Mycoses. 2013. doi:10.1111/myc.12166. 12. Kawachi Y, Ikegami M, Takase T, Otsuka F. Chronically recurrent and disseminated tinea faciei/corporis-autoinoculation from asymptomatic tinea capitis carriage. Pediatr Dermatol. 2010;5:527–8.
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A Chronic Disseminated Dermatophytosis Due to Trichophyton violaceum Ping Zhan • Zhi-hua Li • Chengfang Geng • Qing Jiang • Yun Jin • Somayeh Dolatabadi Weida Liu • G. Sybren de Hoog
•
Received: 13 April 2014 / Accepted: 1 October 2014 / Published online: 17 October 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract A 48-year-old female had presented dandruff and breakable hair for more than 40 years, dry scaly erythema on bilateral palms and feet accompanying with nail destruction for 20 years, and scaling papules on the buttock for 5 years. Direct microscopic examination showed endothrix anthroconidia within broken hair and septate and branched hyphae within skin and nail lesion. Fungal cultures from all infected sites were examined by morphology, ITS sequencing, and random amplified polymorphic DNA fingerprinting, and were identified as Trichophyton violaceum from the same source. The patient was treated with oral terbinafine 0.25 g/day as well as with 1 % terbinafine gel for external use and with 2 % ketoconazole lotion for shampoo and bath. A follow-up after 4 weeks showed that the lesions decreased significantly.
P. Zhan Z. Li C. Geng Q. Jiang Y. Jin Specialized Dermatology Hospital of Jiangxi Province, Nanchang, China P. Zhan W. Liu (&) Department of Mycology, Institute of Dermatology, Chinese Academy of Medical Science and Peking Union Medical College, No. 12 Jiang Wangmiao Street, Nanjing 210042, China e-mail: [email protected] S. Dolatabadi G. S. de Hoog CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands
Keywords Trichophyton violaceum Dermatophytosis Fingerprinting
Introduction Trichophyton violaceum is a common superficial fungus endemic in parts of America, Africa, Europe, and Asia [1–5]. In China, the species is one of the preponderant agents of tinea capitis, mainly being isolated in local regions of Southern and Northwestern China [4, 5]. Other infections caused by T. violaceum, such as tinea corporis, tinea pedis, tinea manuum, and onychomycosis, are infrequently reported [1, 3]. Here, we report a case of disseminated dermatophytosis by T. violaceum which started as tinea capitis 40 years ago and gradually extended to other parts of the body presenting as tinea cruris, tinea pedis, and tinea manus, as well as onychomycosis. Strains from different infected sites were confirmed to be T. violaceum by phenotypic and molecular data, while molecular fingerprinting with random amplified polymorphic DNA (RAPD) confirmed that all isolated strains came from the same source.
Case Report A 48-year-old female from Xinjian area, located nearby Nanchang city, Jiangxi province, South China,
123
160
was admitted to our dermatology clinic with a history of disseminated skin lesions for about 5 years. She had been working as a farmer and was engaged in agricultural production for all her life. As a child 40 years ago, she developed dandruff and fragile hairs with scalp pruritus, which could be relieved mildly by Head & Shoulders shampoo but relapsed quickly. About 20 years ago, her palms and soles began to have a problem of dryness, desquamation, and skin fissures. At the same time, her fingernails and toenails became rough, hyperkeratotic, and crumbled with yellowish to brown discoloration. Five years before admission, her buttocks presented with erythema, papules, and desquamation with pruritus. The lesions had aggravated particularly during the past 2 years. Patient was cachectic but had never sought medical care up to now and denied significant medical problems. The infection was not found in other members of the family who used to live close together in a rural setting. Physical examination revealed a small, cachectic patient (41.2 kg, 148 cm). The hair was dry and dull with isolated scaly patches on the scalp. A few black dots of broken hair could be discerned at close observation. Palms and soles presented a dry, rough, finely fissured surface with onycholysis of the nails. Hyperkeratosis was present around all nails. Scaly, dry erythema with some pin-sized papules could also be seen on both buttocks. No obvious abnormality was found by routine blood examination. Direct microscopic examination of broken hairs revealed endothrix of arthroconidia arranged in chains within hair shafts. Wood’s light examination was negative. Direct microscopy of skin and nail specimens also revealed anthroconidia, as well as short, branched, flexuous hyphae. Samples from eight infected sites (hair, left palm, right palm, left sole, right sole, toenail of right foot, fingernail of left hand, buttocks) were inoculated into Sabouraud’s glucose agar containing chloroamphenicol (50 mg/l) with and without cycloheximide (400 mg/l), incubated at 27 °C. After 1 week, similar colonies presented on all agar slants. They were very slow growing, initially glabrous, moist and waxy, later transforming to become heaped and folded, with a deep violet color. To determine the identity of all strains, genomic DNA was extracted using the ZR Fungal/Bacterial DNA MiniPrepTM Kit (Zymo research, USA), and ITS regions were amplified using ITS1 and ITS4 primers. Sequencing results were blasted in database and
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Mycopathologia (2015) 179:159–161
showed 99 % identity to T. violaceum (CBS 374.92), 98 % to T. soundanese (ATCC 24583), and 98 % to Trichophyton rubrum (CBS 376.49). The T. violaceum-specific microsatellite primers T1 [4] were used, and sequencing results showed to be 99 % in accordance with T. violaceum strain IFM 60448. RAPD was implemented subsequently. Four random primers (M13, T3B, (GGA)7, (CAC)5) were applied using recommended protocols by CBS (http://www.isham. org/members/Protocol/index.asp). Bands of all eight strains proved to be completely consistent, strongly suggesting that the pathogens originated from a common source. The final diagnosis was that of a disseminated tinea by a single strain of T. violaceum. Antifungal susceptibility test was performed using the broth microdilution methods (CLSI M38-A2). Both of the minimum effective concentration of caspofungin and micafungin were 0.06 lg/ml. The minimum inhibitory concentration (MIC)100 of voriconazole, itraconazole, terbinafine, and amphotericin B were 0.06, 0.25, 0.03, and 0.25 lg/ml, respectively. And MIC90 of fluconazole was 2 lg/ml. The patient was treated with terbinafine 0.25 g once a day as well as 1 % terbinafine gel for external use and 2 % ketoconazole lotions for shampoo and bath. The second visit after 4 weeks showed a sufficient decrease of the scalp and skin damage, but no improvement of the nails, and after that, the patients was lost to follow-up.
Discussion Dermatophytes usually involve only a single anatomical area, presenting as localized lesions. Chronic and widespread dermatophyte infections are more often associated with onychomycosis and tinea pedis. Disseminated cutaneous dermatophytosis is also commonly seen in patients with impaired acquired cellular immunity or in patients with immunosuppression [6, 7]. The few reported cases of widespread infection in immunocompetent individuals are mainly caused by the anthropophilic dermatophytes T. rubrum and Trichophyton tonsurans [8–10]. These species are frequently carried asymptomatically and may cause infection after autoinoculation [11, 12]. In our case, the patient was an adult woman with a long history of extensive infection for more than 40 years. She declared to be healthy and refused any other medical
Mycopathologia (2015) 179:159–161
examination. Whether she had immunodeficiency remained unknown. Trichophyton violaceum is an anthropophilic dermatophyte which usually causes chronic and inflammatory skin conditions. The infection is mainly localized on scalp region known as tinea black dot. Tinea corporis may follow after dissemination, and this condition is rarely reported [1, 3]. Transmission and expansion of arthropophilic dermatophytes are impacted by inadequate sanitary conditions, disorders of the immune system (steroid or chronic alcohol abuse, diabetes mellitus, pregnancy, and lymphoproliferative disorders), trauma, and age [10–12]. Dessinioti et al. [11] recently reported 34 cases of asymptomatic scalp carriage (ASC) tinea capitis and found there was a statistically significant association of ASC with T. violaceum. In our previous clinical work, we found several cases of adult tinea capitis presented as seborrheic dermatitis, dandruff, dull hair but without broken hair, or obvious inflammation, and the pathogen in all these cases was identified as T. violaceum [5]. We therefore surmise that T. violaceum is specifically associated with ASC and chronic and repeated infections [12].
References 1. Mapelli ET, Colombo L, Crespi E, Menni S. Toenail onychomycosis due to Trichophyton violaceum complex. (An unusual, emerging localization of this anthropophilic dermatophyle). Mycoses. 2012;2:193–4.
161 2. Hogewoning AA, Adegnika AA, Bouwes Bavinck JN et al. Prevalence and causative fungal species of tinea capitis among schoolchildren in Gabon. Mycoses. 2011;5:e354–9. 3. Romano C, Feci L, Fimiani M. Thirty-six cases of epidemic infections due to Trichophyton violaceum in Siena, Italy. Mycoses. 2013. doi:10.1111/myc.12164. 4. Deng S, Bulmer GS, Summerbell RC, De Hoog GS, Hui Y, Gra¨ser Y. Changes in frequency of agents of tinea capitis in school children from Western China suggest slow migration rates in dermatophytes. Med Mycol. 2008;5:421–7. 5. Li Z, Jin Y, Zhan P et al. The clinical characteristics and pathogens of 117 cases of tinea capitis. Chin J Dermatovenerol. 2012;9:808–809, 841 (in chinese). 6. Jime´nez-Puya R, Va´zquez-Bayo C, Rodriguez-Bujaldo´n A, Go´mez Garcı´a F, Moreno-Gime´nez JC. Extensive tinea in a patient with severe combined immunodeficiency. Pediatr Dermatol. 2009;2:213–4. 7. Budihardja D, Freund V, Mayser P. Widespread erosive tinea corporis by Arthroderma benhamiae in a renal transplant recipient: case report. Mycoses. 2010;53(6):530–2. 8. Balci DD, Cetin M. Widespread, chronic, and fluconazoleresistant Trichophyton rubrum infection in an immunocompetent patient. Mycoses. 2008;6:546–8. 9. de Freitas CF, Mulinari-Brenner F, Fontana HR, Gentili AC, Hammerschmidt M. Ichthyosis associated with widespread tinea corporis: report of three cases. An Bras Dermatol. 2013;4:627–30. 10. Calabro` G, Nino M, La Bella S et al. Trichophyton violaceum infection in an adult black patient in Europe. Int J Dermatol. 2011;6:761–3. 11. Dessinioti C, Papadogeorgaki E, Athanasopoulou V, Antoniou C, Stratigos AJ. Screening for asymptomatic scalp carriage in household contacts of patients with tinea capitis during 1997–2011: a retrospective hospital-based study. Mycoses. 2013. doi:10.1111/myc.12166. 12. Kawachi Y, Ikegami M, Takase T, Otsuka F. Chronically recurrent and disseminated tinea faciei/corporis-autoinoculation from asymptomatic tinea capitis carriage. Pediatr Dermatol. 2010;5:527–8.
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