Dermatophytosis is a common infection observed world- wide and is believed to affect more than 20~25% of the global population¹. In the last 80 years, considerable changes have been observed in dermatophytosis in Korea, including changes in the common causative agents of dermatophytosis and its clinical characteristics. The epidemiology of a dermatophyte infection is influenced by the changing patterns of migration, growth in tourism, host immune competence, pathogenicity of the infectious agent, availability of medical treatment, and changes in the socioeconomic conditions^2-8. Zoonotic diseases can be transmitted between animals and from animals to humans, causing outbreaks among exposed individuals⁹.

Trichophyton verrucosum (T. verrucosum) is a zoophilic fungus known as the primary dermatophyte causing ringworm among cattle in Europe, North America, and other countries. Humans are typically infected via direct contact with the infected cattle, contaminated fomites, or soil; T. verrucosum infection is observed worldwide¹⁰. Kerion celsi caused by T. verrucosum was first reported in the southwestern province of Korea in 1986 by Kim et al.¹¹. Thereafter, several patients have been infected with T. verrucosum in the Young-nam province^12-15. However, recently, the incidence of T. verrucosum infection has been decreasing.

In the present study, we investigated the changes in the epidemiology of T. verrucosum through a retrospective analysis of patient medical records from 2005 to 2017 and compared the data with our previous report on the data from 1986 to 2004.

1. Patients

We performed a retrospective analysis of the medical records of patients who visited the Catholic Skin Clinic and Kyungpook National University Hospital in Daegu from 2005 to 2017. The clinical and epidemiological characteristics of 34 patients infected with T. verrucosum were studied. Furthermore, the medical records were compared with those of 196 patients with T. verrucosum infection between 1986 and 2004. T test was used for the statistical analyses. p < 0.05 was considered to be statistically significant.

2. Methods

Total 34 patients with T. verrucosum were retrospectively reviewed to determine the annual incidence of the infection and its distribution as per age, sex, season, infection site, and place of residence. The diagnosis of T. verrucosum infection was confirmed with macroscopic and microscopic morphological examinations of the cultured colonies. Samples of the fungal examination were obtained by scraping the lesions with a scalpel and culturing them using potato dextrose agar-corn meal Tween 80 media. The cultures were kept at 24~26℃ and examined after 2~4 weeks.

1. Annual incidence

Total 34 patients were diagnosed with T. verrucosum infection (0.00041% among the whole dermatophytosis), and the annual incidence ranged from 0~8 (Table 1). The prevalence of T. verrucosum infection was significantly lower than that in our previous study (p < 0.05), with a decrease in the annual incidence from 10.3 to 2.6 (Figure 1). Although the incidence of T. verrucosum infection was very low, cases are still observed in Korea.

Figure 1. Average annual number of patients with T. verrucosum infection from 1986~2004 and 2005~2017 (T test was used for the statistical analyses)

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2. Age- and sex-based distribution

Of the 34 patients, 17 were men and 17 were women (sex ratio of 1:1) (Table 2). Among them, 14 patients (41.2%) were aged 50~69 years. Of the remaining patients, 6 (17.7%) patients were < 10 years old (Table 2). Our previous study showed that 41.3% of all the patients with T. verrucosum infection were aged < 15 years.

3. Month and season-based distribution

Total 5 patients (14.7%) visited our hospital for the first time in September. Of the 34 patients, 10 each (29.4%) visited the hospital in spring, fall, or winter, representing the lowest incidence in summer (4, 11.8%) (Table 3).

4. Topographical distribution

The most common site for T. verrucosum infection was the arm. Of the 34 patients, 13 (38.2%) had an arm infection (Table 4). The face (9 cases, 26.5%) were the second most common site of infection, while the scalp, back, abdomen, and hip (each 2 cases, each 5.9%) were the third most common sites of infection, followed by the dorsal hand, neck, chest, and leg (each 1 case, each 2.9%) (Table 4). Our previous study reported that the face was the most commonly involved site. Dermatophytosis has several subtypes, depending on the infection site. Tinea corporis was the most common subtype of dermatophytosis caused by T. verrucosum, affecting 22 patients (64.7%) (Table 5). Tinea corporis was defined as dermatophytosis of the neck, chest, back, abdomen, upper and lower extremities, and hip. The second most common subtype was tinea faciei that was observed in 9 patients (26.5%). Tinea capitis was the third most common subtype, affecting 2 patients (5.9%), followed by tinea manus, affecting 1 patient (2.9%) (Table 5).

5. Distribution as per the residential area

Of the 34 patients, 24 (70.6%) lived in rural areas, while 10 lived in urban areas.

T. verrucosum was first described by Sabouraud in 1893¹⁶ and was named by Bodin in 1902¹⁷. Folded, heaped, glabrous, and white colonies are observed in the fungal culture. The fungus grows slowly at room temperature, showing distinct chains of chlamydoconidia in the potassium hydroxide test¹⁸. Wood lamp examination shows positive results in infected cattle and negative results in infected humans. In human infections, positive results are observed only at the early stage of the infection¹⁹.

In cattle, T. verrucosum infection is often observed on the face, periocular area, and scalp as thick scales and hair loss patches. In humans, the infection presents as diffuse inflammation and confluent erythematous annular plaques with severe discharge and kerion celsi. Although T. verrucosum infection is known to be transmitted to humans via contact with infected cattle, there is no definite factor in the infection process that makes it spread¹². In Korea, T. verrucosum was isolated from cattle infected with tinea in 1977 and 1978²⁰. In 1986, human infection was first reported in cattle-farming facilities in Jeon-nam area¹¹. From 1962 to 1974, Korea had imported cattle from countries, such as North America. We believe that T. verrucosum strains in Korea may have entered from countries endemic for this infection. The spreading pathway of T. verrucosum in Japan may be similar to that in Korea²¹.

Since 1986, the prevalence of T. verrucosum infection had been increasing until 2000²². Thereafter, the prevalence has progressively decreased owing to increased awareness regarding the mode of transmission (direct contact with infected cattle) and improved cattle-farming facilities²². This study showed a very low incidence of T. verrucosum infection.

As per our knowledge, susceptibility to T. verrucosum infection is independent of sex and age. Our study also showed similar results with respect to the sex-based distribution. However, age distribution showed a higher incidence of T. verrucosum infection among subjects in their fifties and sixties. Our previous study showed that the highest prevalence of T. verrucosum infection was among those aged < 10 years²². Good health care may be a major reason for the reduction in the prevalence of T. verrucosum infection among children. Takahashi et al.²³ reported a female to male ratio of 1.3:1. George et al.²⁴ reported that T. verrucosum infection was often transmitted within families via contact of contaminated clothes.

The occurrence of T. verrucosum infection is reportedly common in winter and spring, that is, from October to June. In this study, 20 patients (58.8%) were infected during winter or spring, that is, from December to May. The seasonal distribution of T. verrucosum is different from that of T. rubrum. T. rubrum infection is most commonly observed during summer²⁵. The incidence of T. verrucosum infection correlates with that in cattle. Takahashi et al.²³ reported 40 cases in 41 patients from November to April. Aoyagi el al.²⁶ reported 11 cases from December to March, while Kubo et al.²⁷ reported 47 cases, resulting in a total of 58 cases from December to June.

Kubo et al.²⁷ and George et al.²⁴ reported that T. verrucosum infection mainly occurs on the exposed body parts, such as the face, scalp, and upper extremities. Our previous study also reported similar results²². However, we found that the upper extremities were the most common infection site. The higher incidence of T. verrucosum infection among those in their fifties and sixties may explain that the upper extremities were more commonly involved than the face.

T. rubrum infection was checked predominantly in urban areas²⁵; however, T. verrucosum infection was checked in rural areas, because of the exposure to infected cattle. Treatment for T. verrucosum infection includes the administration of oral antifungal agents, such as terbinafine, fluconazole, and griseofulvin, and some topical agents. However, treatment with topical agents alone may require more time and may have lower rates of patient compliance, making it less effective²⁸.

As observed in the present study, the incidence of T. verrucosum infection has changed considerably over the previous 40 years. The gradual decrease in the annual incidence of T. verrucosum infections was prominent from 2000 to 2017. The common causes of dermatophytosis in Korea have been changing owing to increasing public health education and lifestyle diversity. T. verrucosum infection has almost disappeared from Korea; however, there is a possibility of its reappearance. Therefore, public awareness and continuous observation for this organism and infection are crucial. We believe that this study will help dermatologists obtain advanced information regarding the epidemiologic changes with respect to T. verrucosum in Korea.

In relation to this article, We declare that there is no conflict of interest.