Mycopathologia DOI 10.1007/s11046-014-9834-5
Chronically Recurrent and Widespread Tinea Corporis Due to Trichophyton rubrum in an Immunocompetent Patient Q. T. Kong • X. Du • R. Yang • S. Y. Huang H. Sang • W. D. Liu
•
Received: 17 June 2014 / Accepted: 13 November 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract A 31-year-old immunocompetent male who presented with a 4-year history of extensive erythematous and scaly plaques involving the abdomen, gluteal and inguen regions with concomitant tinea pedis and onychomycosis is described. Diagnosis was based on positive mycological examination and positive histopathologic examination. Species identification was performed by growth on Sabouraud dextrose agar and by sequencing of the internal transcribed spacer regions of the rDNA region. The pathogen identified was Trichophyton rubrum. The same fungal species was cultured from his abdominal, gluteal, foot and toenail. A combination therapy with systemic terbinafine and topically applied terbinafine cream was successful. A 1-year follow-up did not show any recurrence of infection.
Introduction
Keywords Chronically Widespread Tinea corporis Trichophyton rubrum Immunocompetent
A 31-year-old male was presented to our department with a 4-year history of recurrent extensive erythematosquamous lesions involving the trunk, gluteal, inguinal and crural regions with concomitant tinea pedis and onychomycosis. The patient stated that the erythematous lesions with slightly scale and pruritus began 7 years earlier on the gluteal and inguinal and the eruptions had disappeared promptly with topical application of 2 % ketoconazole cream. However, he had a 4-year history of repeated recurrence of similar erythra on the gluteal and inguinal. The lesions spread to trunk, lower extremities rapidly after he use a folk prescription. He underwent a 2-week therapy period therapy with systemic terbinafine and miconazole
Q. T. Kong X. Du R. Yang S. Y. Huang H. Sang (&) Jinling Hospital, Department of Dermatology, Nanjing University, School of Medicine, Nanjing 210002, People’s Republic of China e-mail: [email protected] W. D. Liu Institute of Dermatology, Chinese Academy of Medical Sciences, Peking Union Medical College, Nanjing 210042, People’s Republic of China
Chronic, widespread and invasive cutaneous dermatophytoses due to Trichopyhton rubrum are common in immunocompromised patients. In immunocompetent individuals, however, chronic widespread dermatophytoses are more often associated with foot, hand and nail dermatophyte infections and rarely tinea cruris and corporis. We describe a 31-year-old immunocompetent male who presented with a 4-year history of extensive erythematous and scaly plaques involving the abdominal, gluteal and inguen regions with concomitant tinea pedis and onychomycosis.
Case Report
123
Mycopathologia
cream at a local hospital and achieved complete remission, but his rashes developed again after drug discontinuance. In this period, he had used topical corticosteroids on the lesions and traditional Chinese medicine. He had not received any treatment in the last 2 years. He has been healthy except the persistent rashes and denied susceptibility to repeated bacterial or viral infections. There was neither an indication of diabetes nor evidence of using immunosuppressive drugs and corticosteroids. No contact with domesticated or wild animals was reported. There was no history of fungal skin infection in his family. Physical cutaneous examination revealed diffuse erythema on his abdominal, back, gluteal and inguen regions with well-defined borders and scale (Fig. 1). There was also onychauxis on his toenails (Fig. 2). The mucosae were not affected. His laboratory tests including biochemical and serological tests and radiological examinations were all within normal limits. Skin biopsies were taken from his abdomen. The histological picture (Fig. 3) showed epidermal hyperkeratinization. The upper dermis presented a sparse perivascular lymphocytic infiltrate. The PAS stain confirmed the presence of few hyphae in the horny layer. Septate and branching hyphae were observed on direct microscopic examination (KOH preparation) of
Fig. 1 Clinical presentation of the patient
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Fig. 2 Onychauxis of the patient’s toenails
scales obtained by scraping the plaques on the abdominal, gluteal, foot and toenail. Skin-scraping cultures on Sabouraud dextrose agar with chloramphenicol and cycloheximide at 26 °C for 14 days yielded downy white-coloured colonies with crimson pigment on the reverse. Teardrop-shaped microconidias along septate hyphae were established after staining with lactophenol cotton blue on microscopic examination. Genomic DNA was extracted from the three fungal cultures using Biopsin Fungus Genomic DNA Extraction Kit (Bioer Technology, China)
Mycopathologia
Fig. 3 Histological features of the skin biopsy from the abdominal, a HE 9100, b PAS 9400
according to the manufacturer’s protocol. The universal fungal primer pair was used for amplification: ITS1 (50 -TCCGTAGGTGAACCTGCGG-30 ) and ITS4 (50 -TCCTCCGCTTATTGATATGC-30 ). The PCR assay was performed, and the PCR product was directly sequenced using both the ITS1 primer and ITS4 primer. The resultant nucleotide sequences were aligned to produce consensus for analysis. The consensus sequence of the isolate aligned with 99 % sequence similarity to multiple sequences of T. rubrum available in the GenBank database. Moreover, we identified the genotype of the four isolated strains using primers TrNTSF-2(50 -ACCGTATTAAGCT AGCGCTGC-30 ) and TrNTSR-4 (50 -TGCCACTTCGATTAGGAGGC-30 ) [1] and random amplified polymorphic DNA methods. Amplification products were separated by electrophoresis in 1.5 % agarose gels and photographed. The results showed that the four isolated strains were the same fungal species (Fig. 4). The fungal culture and PCR approach resulted in the identification of T. rubrum. The sequences of the isolates from abdomen and toenail in this publication have been submitted to Genbank (accession numbers KP012333, KP012334). And the
Fig. 4 Amplification of the TRS-1 subrepeat element for clinical isolates. (1) The isolate from abdominal, (2) inguen, (3) gluteal and (4) toenail
123
Mycopathologia
two isolates have been deposited in the Institute of Dermatology, Chinese Academy of Medical Sciences, Chinese Medical Fungi Culture Collection Center, Nanjing, China under accession number CMCC (T1j and T1k, respectively). In vitro antifungal susceptibility testing was performed in accordance with CLSIM38-P. The most sensitive antifungal drug against our strain was terbinafine, followed by itraconazole. Therefore, treatment was started with oral terbinafine (250 mg/day) as well as local therapy with terbinafine cream once a day for 1 month. After treatment, the skin lesions had cleared up (Fig. 5) and mycological examination was negative. Treatment with oral terbinafine was maintained during 12 weeks. A follow-up examination 1 year later showed no recurrence of symptoms.
Discussion Trichophyton rubrum is the most common cause worldwide for superficial dermatophytosis. Chronic and widespread infections often occur in immunocompromised patients, such as those with AIDS. There have been a few reports of widespread tinea corporis in
immunocompetent patients caused by T. rubrum, which may persist for several years [2–4]. Our case presented here is unique in that the patient was immunocompetent and had a 7-year history of chronic recurrent multiple of corporis despite intermittent topical and system antifungal treatment. The lesions of our patient began 7 years earlier on the gluteal and inguinal, followed by spread to trunk, lower extremities and toenail gradually, and repeated recurrence. However, he did not get a professional diagnosis and treatment. From his medical history, he had used topical corticosteroids on the lesions and traditional Chinese medicine. This may be one of the most causes of our patient’s lesions progression. Regard to chronic, widespread and recurrent cutaneous dermatophytoses, it is important to identify the isolation pathogen from patients. The fungus was identified as T. rubrum based on both macroscopic features of colonies, microscopic characteristics on lactophenol cotton blue staining and PCR approach results. Moreover, the isolation of T. rubrum from his toenail is the same species from his abdomen, gluteal and foot. Therefore, the chronic recurrent tinea corporis in this case is likely due to repeated autoinfection with pathogenic dermatophytes from the
Fig. 5 Almost complete healing of the lesions 1 month after the treatment
123
Mycopathologia
patient’s toenail, which served as a reservoir for the pathogen. Moreover, Mannans in the cell walls of dermatophytes have immuno-inhibitory effects. In T. rubrum, the mannans may also decrease epidermal proliferation, thereby decreasing the likelihood of the fungus being sloughed off prior to invasion. This mechanism is thought to contribute to the chronicity of infections caused by T. rubrum [5]. In a long period of treatment, the pathogen may be resistance to antifungal agents. Therefore, drug sensitivity test is important to choose antifungal agents. The isolation was identified as T. rubrum; according to the results of drug sensitivity test, systemic terbinafine was given and our patient showed rapid improvement and clearing of the cutaneous lesions. In conclusion, we have described a rare form of chronic and widespread tinea infection caused by T. rubrum in an immunocompetent patient. The observations in our case indicate the importance of surveying the nails as a potential source of pathogenic
dermatophytes in patients with recurrent and widespread tinea corporis. Acknowledgments This work was supported by the National Natural Science Foundation of China (Grant No. 81371782).
References 1. 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. 2. Gorani A, Schiera A, Oriani A. Case report. Widespread tinea corporis due to Trichophyton rubrum. Mycoses. 2002;45:195–7. 3. Vittorio CC. Widespread tinea corporis in an immunocompetent patient resistant to all conventional forms of treatment. Cutis. 1997;60:283–5. 4. Balci DD, Cetin M. Widespread, chronic, and fluconazoleresistant Trichophyton rubrum infection in an immunocompetent patient. Mycoses. 2008;51:546–8. 5. Almeida SR. Immunology of dermatophytosis. Mycopathologia. 2008;166:277–83.
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Chronically Recurrent and Widespread Tinea Corporis Due to Trichophyton rubrum in an Immunocompetent Patient Q. T. Kong • X. Du • R. Yang • S. Y. Huang H. Sang • W. D. Liu
•
Received: 17 June 2014 / Accepted: 13 November 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract A 31-year-old immunocompetent male who presented with a 4-year history of extensive erythematous and scaly plaques involving the abdomen, gluteal and inguen regions with concomitant tinea pedis and onychomycosis is described. Diagnosis was based on positive mycological examination and positive histopathologic examination. Species identification was performed by growth on Sabouraud dextrose agar and by sequencing of the internal transcribed spacer regions of the rDNA region. The pathogen identified was Trichophyton rubrum. The same fungal species was cultured from his abdominal, gluteal, foot and toenail. A combination therapy with systemic terbinafine and topically applied terbinafine cream was successful. A 1-year follow-up did not show any recurrence of infection.
Introduction
Keywords Chronically Widespread Tinea corporis Trichophyton rubrum Immunocompetent
A 31-year-old male was presented to our department with a 4-year history of recurrent extensive erythematosquamous lesions involving the trunk, gluteal, inguinal and crural regions with concomitant tinea pedis and onychomycosis. The patient stated that the erythematous lesions with slightly scale and pruritus began 7 years earlier on the gluteal and inguinal and the eruptions had disappeared promptly with topical application of 2 % ketoconazole cream. However, he had a 4-year history of repeated recurrence of similar erythra on the gluteal and inguinal. The lesions spread to trunk, lower extremities rapidly after he use a folk prescription. He underwent a 2-week therapy period therapy with systemic terbinafine and miconazole
Q. T. Kong X. Du R. Yang S. Y. Huang H. Sang (&) Jinling Hospital, Department of Dermatology, Nanjing University, School of Medicine, Nanjing 210002, People’s Republic of China e-mail: [email protected] W. D. Liu Institute of Dermatology, Chinese Academy of Medical Sciences, Peking Union Medical College, Nanjing 210042, People’s Republic of China
Chronic, widespread and invasive cutaneous dermatophytoses due to Trichopyhton rubrum are common in immunocompromised patients. In immunocompetent individuals, however, chronic widespread dermatophytoses are more often associated with foot, hand and nail dermatophyte infections and rarely tinea cruris and corporis. We describe a 31-year-old immunocompetent male who presented with a 4-year history of extensive erythematous and scaly plaques involving the abdominal, gluteal and inguen regions with concomitant tinea pedis and onychomycosis.
Case Report
123
Mycopathologia
cream at a local hospital and achieved complete remission, but his rashes developed again after drug discontinuance. In this period, he had used topical corticosteroids on the lesions and traditional Chinese medicine. He had not received any treatment in the last 2 years. He has been healthy except the persistent rashes and denied susceptibility to repeated bacterial or viral infections. There was neither an indication of diabetes nor evidence of using immunosuppressive drugs and corticosteroids. No contact with domesticated or wild animals was reported. There was no history of fungal skin infection in his family. Physical cutaneous examination revealed diffuse erythema on his abdominal, back, gluteal and inguen regions with well-defined borders and scale (Fig. 1). There was also onychauxis on his toenails (Fig. 2). The mucosae were not affected. His laboratory tests including biochemical and serological tests and radiological examinations were all within normal limits. Skin biopsies were taken from his abdomen. The histological picture (Fig. 3) showed epidermal hyperkeratinization. The upper dermis presented a sparse perivascular lymphocytic infiltrate. The PAS stain confirmed the presence of few hyphae in the horny layer. Septate and branching hyphae were observed on direct microscopic examination (KOH preparation) of
Fig. 1 Clinical presentation of the patient
123
Fig. 2 Onychauxis of the patient’s toenails
scales obtained by scraping the plaques on the abdominal, gluteal, foot and toenail. Skin-scraping cultures on Sabouraud dextrose agar with chloramphenicol and cycloheximide at 26 °C for 14 days yielded downy white-coloured colonies with crimson pigment on the reverse. Teardrop-shaped microconidias along septate hyphae were established after staining with lactophenol cotton blue on microscopic examination. Genomic DNA was extracted from the three fungal cultures using Biopsin Fungus Genomic DNA Extraction Kit (Bioer Technology, China)
Mycopathologia
Fig. 3 Histological features of the skin biopsy from the abdominal, a HE 9100, b PAS 9400
according to the manufacturer’s protocol. The universal fungal primer pair was used for amplification: ITS1 (50 -TCCGTAGGTGAACCTGCGG-30 ) and ITS4 (50 -TCCTCCGCTTATTGATATGC-30 ). The PCR assay was performed, and the PCR product was directly sequenced using both the ITS1 primer and ITS4 primer. The resultant nucleotide sequences were aligned to produce consensus for analysis. The consensus sequence of the isolate aligned with 99 % sequence similarity to multiple sequences of T. rubrum available in the GenBank database. Moreover, we identified the genotype of the four isolated strains using primers TrNTSF-2(50 -ACCGTATTAAGCT AGCGCTGC-30 ) and TrNTSR-4 (50 -TGCCACTTCGATTAGGAGGC-30 ) [1] and random amplified polymorphic DNA methods. Amplification products were separated by electrophoresis in 1.5 % agarose gels and photographed. The results showed that the four isolated strains were the same fungal species (Fig. 4). The fungal culture and PCR approach resulted in the identification of T. rubrum. The sequences of the isolates from abdomen and toenail in this publication have been submitted to Genbank (accession numbers KP012333, KP012334). And the
Fig. 4 Amplification of the TRS-1 subrepeat element for clinical isolates. (1) The isolate from abdominal, (2) inguen, (3) gluteal and (4) toenail
123
Mycopathologia
two isolates have been deposited in the Institute of Dermatology, Chinese Academy of Medical Sciences, Chinese Medical Fungi Culture Collection Center, Nanjing, China under accession number CMCC (T1j and T1k, respectively). In vitro antifungal susceptibility testing was performed in accordance with CLSIM38-P. The most sensitive antifungal drug against our strain was terbinafine, followed by itraconazole. Therefore, treatment was started with oral terbinafine (250 mg/day) as well as local therapy with terbinafine cream once a day for 1 month. After treatment, the skin lesions had cleared up (Fig. 5) and mycological examination was negative. Treatment with oral terbinafine was maintained during 12 weeks. A follow-up examination 1 year later showed no recurrence of symptoms.
Discussion Trichophyton rubrum is the most common cause worldwide for superficial dermatophytosis. Chronic and widespread infections often occur in immunocompromised patients, such as those with AIDS. There have been a few reports of widespread tinea corporis in
immunocompetent patients caused by T. rubrum, which may persist for several years [2–4]. Our case presented here is unique in that the patient was immunocompetent and had a 7-year history of chronic recurrent multiple of corporis despite intermittent topical and system antifungal treatment. The lesions of our patient began 7 years earlier on the gluteal and inguinal, followed by spread to trunk, lower extremities and toenail gradually, and repeated recurrence. However, he did not get a professional diagnosis and treatment. From his medical history, he had used topical corticosteroids on the lesions and traditional Chinese medicine. This may be one of the most causes of our patient’s lesions progression. Regard to chronic, widespread and recurrent cutaneous dermatophytoses, it is important to identify the isolation pathogen from patients. The fungus was identified as T. rubrum based on both macroscopic features of colonies, microscopic characteristics on lactophenol cotton blue staining and PCR approach results. Moreover, the isolation of T. rubrum from his toenail is the same species from his abdomen, gluteal and foot. Therefore, the chronic recurrent tinea corporis in this case is likely due to repeated autoinfection with pathogenic dermatophytes from the
Fig. 5 Almost complete healing of the lesions 1 month after the treatment
123
Mycopathologia
patient’s toenail, which served as a reservoir for the pathogen. Moreover, Mannans in the cell walls of dermatophytes have immuno-inhibitory effects. In T. rubrum, the mannans may also decrease epidermal proliferation, thereby decreasing the likelihood of the fungus being sloughed off prior to invasion. This mechanism is thought to contribute to the chronicity of infections caused by T. rubrum [5]. In a long period of treatment, the pathogen may be resistance to antifungal agents. Therefore, drug sensitivity test is important to choose antifungal agents. The isolation was identified as T. rubrum; according to the results of drug sensitivity test, systemic terbinafine was given and our patient showed rapid improvement and clearing of the cutaneous lesions. In conclusion, we have described a rare form of chronic and widespread tinea infection caused by T. rubrum in an immunocompetent patient. The observations in our case indicate the importance of surveying the nails as a potential source of pathogenic
dermatophytes in patients with recurrent and widespread tinea corporis. Acknowledgments This work was supported by the National Natural Science Foundation of China (Grant No. 81371782).
References 1. 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. 2. Gorani A, Schiera A, Oriani A. Case report. Widespread tinea corporis due to Trichophyton rubrum. Mycoses. 2002;45:195–7. 3. Vittorio CC. Widespread tinea corporis in an immunocompetent patient resistant to all conventional forms of treatment. Cutis. 1997;60:283–5. 4. Balci DD, Cetin M. Widespread, chronic, and fluconazoleresistant Trichophyton rubrum infection in an immunocompetent patient. Mycoses. 2008;51:546–8. 5. Almeida SR. Immunology of dermatophytosis. Mycopathologia. 2008;166:277–83.
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