Trichophyton erinacei is a zoophylic dermatophyte, member of the Trichophyton mentagrophytes complex, known to cause superficial skin infections in humans. Usually, it is carried by the 17 species of terrestrial hedgehogs, either as an infection or as asymptomatic carriers   . Terrestrial hedgehogs (Atelerix albiventris) have more often become attractive animals to have as pets, but they also transmit several zoonosis, including salmonellosis, mycobacteriosis, and protozoan infections like Cryptosporidium parvum  , but mainly dermatophytosis. Mycoses transmitted by hedgehogs include mainly tinea manuum  , and occasionally tinea capitis, kerion celsi  , tinea barbae  , tinea faciei, and tinea corporis  .
Human infection by T. erinacei occurs by direct contact with the hedgehog, or through abrasions or wounds. About 76% of cases involve the extremities, specially hands and wrists     . Clinically, it presents as unilateral, erythematous, scaly cutaneous plaques with variable vesicles, pustules, and erosions     . These infections occur worldwide. The first case was described in New Zealand  , followed later by cases from United Kingdom, Western Europe, and more recently, Japan and Korea  . In Mexico, a previous case was reported  . Herein, we present a case of inflammatory tinea manuum due to Trichophyton erinacei from a pet hedgehog.
2. Case Report
A 22 year-old male student complained of a 1-month history of skin lesions on his right hand. The patient does not remember a history of trauma. A general physician treated him with topical antibiotics and steroids with mild temporal improvement.
In the physical examination, there were 3 erythematous scaly exudative plaques measuring between 2 × 2 cm and 1 × 1.5 cm on his right 5th finger (Figure 1). We suspected an infection and samples were obtained for bacterial, mycobacterial, and fungal cultures. KOH examination revealed hyphae compatible with dermatophytes. The bacterial and mycobacterial cultures were negative. Mycologic culture in Sabouraud Dextrose Agar (SDA) incubated at 28˚C grew a flat, white, dusty colony with elevated center. Microscopic examination of the colony sample contrasted with methilene blue showed thin branched filaments, some curved, with multiple sessile, microconidia compatible with Trichophyton sp. In a second medical consultation the patient stated that he had a pet African hedgehog (Atelerix albiventis). KOH microscopic examination of hedgehog’s scales showed abundant hyphae but culture in SDA was negative. With this background the dermatophyte was studied by morphological and molecular techniques.
3. Morphologic Study
A sample from the positive culture was re-cultured in Casamino Acids agar and Borelli agar for microscopic and macroscopic morphologic study (Figure 2 and Figure 3). The urease test was positive after 4 days.
1) Molecular study
A sample from monosporic culture was placed on Dextrose Sabouraud Broth for 5 days at 28˚C at 90 rpm. DNA was extracted using the Exgene Plant SV mini kit (GeneAll, Biotechnology, Korea). PCR was performed to amplify the
Figure 1. Erythematous pustular and eroded plaque on the 5th right finger caused by Trichophyton erinacei, in a male patient infected through contact with his pet hedgehog.
Figure 2. Trichophyton erinacei culture in various media after 12 days at 28˚C. CAA: Casamino Acids agar. Ivory white granular colony with slight yellow pigment in the reverse. BO: Borelli agar. Granular colony with cotton-like central elevation and remarkable yellow pigment in the reverse. SDA: Sabouraud dextrose agar. White granular colony with elevated center and slight brown pigment in the reverse side.
ITS1-5.8S-ITS2 region of the ribosomal RNA. In a 50 µL final volume, the reaction mixture contained 100 ng of DNA, buffer 1X, Taq DNA polymerase (recombinant) 3.5 U, MgCl2 2 mM, dNTPs 0.25 mM (Thermo Fisher Scientific, USA); oligonucleotides ITS1 (5’-TCC GTA GGT GAA CCT GCG G-3’) and ITS4 (5’-TCC TCC GCT TAT TGA TAT GC-3’)  (Merck, Germany). The cycles and temperatures were as follows: one 5-min cycle at 96˚C, forty cycles of 94˚C, 30 s, 58˚C, 30 s and 72˚C, 30 s. In addition, a final cycle at 72˚C, 5 min.
Figure 3. Microscopic aspect of Trichophyton erinacei grown in ADS and stained with lactophenol blue. A: Thick and erect hyphae with abundant round conidia. (Scale: 10 µm). B: Smooth and thin wall macroconidium, with several septa (Scale 5 µm). C: Abundant round conidia with thick hyphae and vesicular structures (arrow) (Scale 5 µm). D: Thick hyphae with long pyriform conidia (arrow) (Scale 5 µm).
The resulting amplicon (700 pb) was visualized in 1.5% agarose gel, stained with GelRed (Biotium, USA), and purified with the DNA Clean and ConcentratorTM-5 kit (Zymo Research, USA) for sequencing. (Figure 4) The resulting sequence was compared with the GenBank (https://www.ncbi.nlm.nih.gov; August 13, 2018). Analysis indicated 100% identity with 10 strains of Trichophyton erinacei, and 11 of Arthroderma benhamiae (sexual form of T. erinacei).
After gathering all the clinical, mycologic, and molecular findings, the final diagnosis was inflammatory tinea manuum due to Trichophyton erinacei acquired from a pet hedgehog (Atelerix albiventris). Clinical and mycologic cure was achieved after treatment with terbinafine 250 mg P.O. daily for 30 days. Only a residual erythematous macule remained (Figure 5).
2) Sensitivity to antifungals
In vitro susceptibility testing using the microdilution broth method according to the M38-A2 guidelines showed resistance to fluconazole and the following MIC levels: itraconazole 0.5 µg/mL, posaconazole 0.03 µg/mL, fluconazole 64 µg/mL, voriconazole 0.06 µg/mL, amphotericin B 4 µg/mL, terbinafine 0.06 µg/mL and ciclopirox olamine 0.25 µg/mL.
Figure 4. PCR product electrophoresed in a 1.5% agarose gel. The product size is about 700 bp which was purified and sent for sequencing. M: Molecular weight marker 100 bp; 1: T. erinacei amplicon; 2: Negative PCR control.
Figure 5. Lesion clinical appearance after treatment with oral terbinafine for 30 days. Residual erythema is only observed.
Trichophyton erinacei (J.M.B. Sm. & Marples; Quaife 1966) is a zoophilic dermatophyte whose natural host is the hedgehog. The rate of infection in humans is 20% - 47%  . A medline and Scopus search up until October 29, 2018, revealed 30 reports (mostly reviews) with 54 cases in humans    . The first case was reported by Smith & Marples in 1963  . Contact with African hedgehogs is a common trait. Of the 54 cases reported in the literature, 58.6% had contact with a hedgehog, and 13.7% with guinea pigs. The remaining cases have been acquired from the soil   or humans  . In our case, authors consider hedgehog as the infection source, as in the direct examination of scales, many fungal filaments were observed, despite culture was negative. Usually, there are single lesions, but several cases had 2 or 3 separate body areas affected   . Some cases have presented as Kerion   . In Mexico, Lammoglia et al. reported the case of a 31-year-old male with tinea incognito and Majocchi’s granuloma by T. erinacei from a hedgehog, treated successfully with terbinafine 250 mg P.O. daily for 6 weeks  . Herein, we have presented the second case from Mexico.
The differential diagnosis of any inflammatory tinea on hands or feet includes dyshidrotic eczema and contact dermatitis. Molecular testing is necessary to confirm the etiologic diagnosis of tineas, including sequencing the ITS region of ribosomal DNA and morphologic studies      .
Treatment of extensive lesions (hyperkeratotic, inflammatory, folliculitis) requires systemic terbinafine or itraconazole for 1 - 12 weeks     . Topical treatment with imidazoles, allylamines, and morpholines is useful for superficial cases, in pregnant or lactating women, or if significant oral drug interactions exist. Cure rates are approximately 80%. Additionally, topical treatment is given as an adjuvant during oral therapy, and to prevent recurrence after systemic therapy   . It is important to treat the hedgehog too, even if it is asymptomatic   .
In our knowledge there are no reports of in vitro antifungal susceptibility studies for T. erinacei. In this study a high MIC for amphotericin B (4 µg/mL) and a resistance level for fluconazole (64 µg/mL) were found. Our patient was successfully treated with terbinafine (250 mg/day), a drug that showed a high in vitro susceptibility.
The African pygmy hedgehog (Atelerix albiventris), member of the family Erinaceidae, is widely known as the four-toed hedgehog. In recent years, these hedgehogs have become popular as domestic pets all over the world. Several studies in these animals have shown the presence of T. erinacei in their scales or spines without clinical manifestations, but there are also cases in which severe infectious symptoms caused by this dermatophyte are reported  .
It is increasingly common to have exotic pets in the home, which represent a potential source of zoonotic infection. Here, we present the second Mexican case of an inflammatory tinea of the hand, whose etiology was determined by morphology and PCR-sequencing as Trichophyton erinacei. It is important to make a detailed clinical history to support the possible source of infection and etiology of an inflammatory dermatophytosis.
We thank Dr. Patricia Manzano-Gayosso for performing suceptibility testing (Department of Microbiology and Parasitology, School of Medicine, National Autonomous University of Mexico), and Dr. Carlos Garcia Rementeria for the translation of the text.
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