Dermatophytoses are transmissible infections that affect one billion people worldwide and have a significant impact on public health. Dermatophytes distribution evolves geographically and over time. Consequently, local epidemiology should be periodically assessed to control infection.
AimsTo describe the local distribution of dermatophytes and types of dermatophytosis through the analysis of samples from patients with suspected superficial mycoses, and to identify areas of improvement.
MethodsA retrospective epidemiological analysis of mycological culture results from skin, hair and nail samples referred to the mycology lab in the Hospital Clínico Universitario Lozano Blesa, Zaragoza (Spain) between 2020 and 2023 was performed, and the results statistically analyzed.
Results4371 specimens (skin: 41.4%; hair: 5.1%; nails: 53.5%) were cultured using standard procedures. The demand for testing increased by 53% over a 4-year time period and a dermatophyte positivity rate of 16.7% (n=731) was found. The species distribution was the following: Trichophyton rubrum (56%), Trichophyton tonsurans (11.3%), Microsporum canis (11.8%), Trichophyton interdigitale (7%), Trichophyton. mentagrophytes (5.8%), Microsporum audouinii (3.8%) and other species (4.9%), with an anthropophilic to zoophilic ratio of 4:1. The dermatophytoses clinical forms found were tinea unguium (39.6%), associated to population over 45 years, tinea corporis (24.7%) and tinea capitis (10.6%), both associated to people with less than 16 years group, tinea pedis (17.5%), mainly observed in people aged 31–45 years; other forms accounted for 7.6%. Finally, the Emergency department requested 11.9% of the mycological tests.
ConclusionsLocal epidemiology of dermatophytoses highlights the predominance of anthropophilic species, whereas 35 years ago zoophilic species represented 80% of the isolates. Interestingly, mild superficial lesions are frequently and inappropriately brought to the Emergency department.
Las dermatofitosis son infecciones transmisibles con impacto en la salud pública al afectar globalmente a más de 1000 millones de personas. Analizar periódicamente la epidermiología local ayuda a controlar la infección, ya que la distribución de los dermatofitos cambia continuamente.
ObjetivosDescribir la distribución local de los dermatofitos y las dermatofitosis mediante el análisis de muestras superficiales con sospecha de micosis e identificar áreas de mejora en su diagnóstico.
MétodosSe realizó, mediante análisis estadístico, un estudio epidemiológico retrospectivo de las muestras de piel, pelo y uñas cultivadas en el laboratorio de micología del Hospital Clínico Universitario Lozano Blesa, Zaragoza, (España) durante el periodo 2020-2023.
ResultadosSe cultivaron 4371 muestras de piel (41.4%), pelo (5,1%) y uñas (53,5%) según procedimientos estandarizados. La demanda de peticiones aumentó un 53% en 4 años. La tasa de positividad para dermatofitos fue del 16,7% (n=731). Las especies aisladas fueron Trichophyton rubrum (56%), Trichophyton tonsurans (11,3%), Microsporum canis (11,8%), Trichophyton interdigitale (7%), Trichophyton mentagrophytes (5,8%), Microsporum audouinii (4%) y otras (4,9%). La proporción de especies antropofílicas/zoofílicas fue de 4:1. Las formas clínicas observadas fueron tinea unguium (39,6%) asociada a mayores de 45 años, tinea corporis (24,7%) y tinea capitis (10,6%), ambas asociadas a menores de 16 años, y tinea pedis (17,5%), asociada al grupo de 31-45 años. Otras formas clínicas representaron el 7,6%. El Servicio de Urgencias solicitó el 11,9% de las peticiones.
ConclusionesLas dermatofitosis causadas por especies antropofílicas predominan en Zaragoza actualmente; en 1997, el 80% eran zoofílicas. Se ha observado un uso inadecuado del servicio de Urgencias para el diagnóstico de lesiones dermatológicas superficiales.
Dermatophytosis, tinea or ringworm are alternative terms referring to the infection caused by dermatophytes, a group of ascomycetous fungi belonging to the Order Onygenales. Dermatophytes are keratinophilic fungi capable of exploiting keratin-rich tissues such as skin, nails or hair. Traditionally, dermatophytes have been classified into three types, anthropophilic, zoophilic and geophilic according to their environmental niche: humans, non-human animals or soil, respectively. Infection can occur by direct contact with an infected individual or via an indirect exposure to viable arthroconidia from the environment or on fomites.
Recently, the Global Burden of Fungal Disease study estimated that cutaneous fungal infections are the fourth most common health problem, affecting one billion people worldwide.2 A 2015 study in Spain calculated the national burden of superficial mycosis as 6,721,000 infected individuals in an estimated total population of 47,000,000.11
Dermatophytes distribution depends on several geographic, environmental and socioeconomic variables. Changes in human lifestyle or the environment, population migratory fluxes and the increasingly widespread use of antimicrobial drugs in human medicine, in farming and in intensive agriculture have modified the epidemiology of fungal infections over recent decades.16
This work aims to describe the epidemiology of dermatophytoses in the Sector Sanitario Zaragoza III (Zaragoza Healthcare Area III) which oversees a geographical region of 6000km2 in the north and northwest area of Zaragoza province (Spain), providing healthcare services to 320,858 inhabitants. Understanding the local dynamics of dermatophytes would help to implement public health measures aimed at controlling their transmission. Hence, the present research aims to identify any diagnostic pitfalls or areas for improvement. In addition, this study will enable us to identify weaknesses in the implemented diagnostic procedure, helping us to improve our protocols and the efficiency of the healthcare system.
MethodsAn epidemiological, descriptive and retrospective study to analyze all dermatophytosis cases diagnosed by culture in the period January 1st 2020 to December 31st 2023 at the University Hospital Lozano Blesa in Zaragoza (Spain), has been performed.
Skin scales, hair and nail scrapings were referred to the Department of Microbiology for mycological analysis. Samples were cultured on commercial Sabouraud Agar plates supplemented with gentamicin and chloramphenicol (SGC2) (bioMérieux, France) and Dermatophyte Test Medium (DTM) (Maim SL, Spain). Plates were incubated for 15 days at 30°C. Fungi from positive cultures were sub-cultured on in-house Potato Dextrose Agar (PDA) plates (VWR International, Belgium) and submitted to MALDI-TOF mass spectrometry identification (Bruker Daltonics, Germany) using the Filamentous Fungi Library 3.0. Identification with MALDI-TOF was used to provide a preliminary report (“dermatophyte in identification”). Culture macroscopic features of the fungal isolates and lactophenol blue preparations for direct light microscopy were used to achieve a definitive identification at species level following the Atlas of Clinical Fungi descriptions.8
The Lab Information System (LIS) Modulab (Werfen, Spain) was used to extract test-request data. Patients’ clinical history records were also consulted whenever relevant clinical data had been omitted. The variables included were age (≤15 years; 16–30; 31–45; 46–60 and >60 years), gender, specimen type, suspected clinical form of tinea, year of request, type of healthcare provider requesting the tests, culture result and isolated dermatophyte species.
For the statistical analysis, IBM SPSS Statistics 29 software was used. Pearson's Chi square test was applied to study the association between the selected categorical variables, and a p-value≤0.05 was considered statistically significant. When significance was found, Cramer's V test was applied to determine the strength of the association between those categorical variables, considering the following interpretation: weak (<0.1), moderate (0.1–0.3) and strong (>0.3).
This study was approved by the Research Ethics Committee (CEICA) on 4th December 2024. Dossier number: C.I. PI24/376.
ResultsDuring the study period, a total of 4371 samples from 3696 patients were referred to the Mycology lab to diagnose suspected cases of superficial mycoses. Of those, 5.1% were hair samples, 41.4% skin scales and 53.5% nail scrapings. Dermatophytes were isolated from 731 samples, resulting in a global positivity rate for dermatophytes of 16.7%. The number of requests for mycological assays increased 53% over the study period, with nail specimens experiencing the greatest increase in numbers. After ruling out duplicate and positive follow-up control cultures, 652 patients were diagnosed with dermatophytosis, see Table 1.
Dermatological superficial samples collected according to specimen type and year, and dermatophyte positivity.
| Specimen | 2020 | 2021 | 2022 | 2023 | Total |
|---|---|---|---|---|---|
| Hair | 68 (7.6%)a | 41 (4.1%) | 51 (4.6%) | 63 (4.6%) | 223 (5.1%) |
| Skin scales | 425 (47.5%)a | 442 (41.9%)a | 463 (41.9%) | 481 (35.1%)a | 1811 (41.4%) |
| Nail scrapings | 401 (44.9%)a | 518 (51.7%) | 591 (53.5%) | 827 (60.3%) | 2337 (53.5%) |
| Total (n) | 894 | 1001 | 1105 | 1371 | 4371 |
| Chi2=62,414 (>0.001); Cramer's V=0.084 | |||||
| Dermatophyte positivity rate | 158 (17.7%) | 161 (16.1%) | 196 (17.7%) | 216 (15.8%) | 731 (16.7%) |
The fungal species recovered and the types of tinea diagnosed are summarized in Table 2. In the healthcare area, Trichophyton rubrum was the most prevalent dermatophyte, being responsible for 56% cases of tinea. Other frequently occurring species identified include Microsporum canis (11.8%), Trichophyton tonsurans (11.3%), Trichophyton interdigitale (7.1%), Trichophyton mentagrophytes (5.8%) and other species (4.9%). The ratio of anthropophilic-to-zoophilic species was 4:1. In terms of clinical presentation, tinea unguium (39.6%) was the most frequently reported, followed by tinea corporis (24.7%), tinea pedis (17.5%), tinea capitis (10.6%) and other forms (7.6%). Noteworthily, the statistical analysis demonstrated that T. tonsurans and M. canis were associated to both skin and hair samples, while significant associations were also found between Microsporum audouinii and hair samples, T. mentagrophytes and skin, and both T. rubrum and T. interdigitale to nail scrapings (see Table 3).
Number of dermatophyte isolates recovered according to species and the clinical form of tinea diagnosed.
| Clinical form | Tinea capitis | Tinea corporis | Tinea cruris | Tinea manuum | Tinea pedis | Tinea unguium | No data | N (%) |
|---|---|---|---|---|---|---|---|---|
| Dermatophytes | ||||||||
| Zoophilic | ||||||||
| Microsporum canis | 20 | 53 | 1 | 0 | 0 | 0 | 3 | 77 (11.8%) |
| Trichophyton mentagrophytes | 3 | 21 | 0 | 1 | 5 | 7 | 1 | 38 (5.8%) |
| Trichophyton equinum | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 1 (0.1%) |
| Anthropophilic | ||||||||
| Epidermophyton floccosum | 0 | 0 | 0 | 0 | 2 | 2 | 0 | 4 (0.6%) |
| Microsporum audouinii | 13 | 6 | 1 | 0 | 2 | 3 | 0 | 25 (3.8%) |
| Microsporum ferrugineum | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 1 (0.1%) |
| Trichophyton interdigitale | 0 | 4 | 0 | 3 | 11 | 28 | 0 | 46 (7%) |
| Trichophyton rubrum | 6 | 44 | 18 | 10 | 85 | 200 | 2 | 365 (56%) |
| Trichophyton soudanense | 5 | 0 | 0 | 1 | 0 | 1 | 0 | 7 (1.1%) |
| Trichophyton tonsurans | 17 | 26 | 4 | 4 | 8 | 15 | 0 | 74 (11.3%) |
| Trichophyton violaceum | 1 | 0 | 0 | 0 | 1 | 1 | 0 | 3 (0.4%) |
| Geophilic | ||||||||
| Nannizzia gypsea | 1 | 1 | 1 | 0 | 0 | 0 | 0 | 3 (0.4%) |
| Other dermatophytes | 3 | 4 | 0 | 0 | 0 | 1 | 0 | 8 (1.2%) |
| N (%) | 69 (10.6%) | 161 (24.7%) | 25 (3.8%) | 19 (2.9%) | 114 (17.5%) | 258 (39.6%) | 6 (0.9%) | 652 |
Percentage of dermatophytoses classified per specimen type and the species isolated.
| Dermatophyte species | Specimen type | Total | ||
|---|---|---|---|---|
| Hair | Skin | Nail | ||
| Microsporum audouini | 19.2%a | 3.5% | 1.2% | 3.8% |
| Microsporum canis | 28.8%a | 18%a | 0% | 11.8% |
| Trichophyton interdigitale | 0% | 5.5% | 10.5%a | 7.1% |
| Trichophyton mentagrophytes | 3.8% | 8.4%a | 2.7% | 5.8% |
| Trichophyton rubrum | 9.6% | 46.8% | 77.7%a | 56% |
| Trichophyton tonsurans | 23.1%a | 13.7%a | 5.9% | 11.3% |
| Other dermatophytes | 15.4% | 4.1% | 2% | 4.1% |
| Total patients (N) | 52 | 344 | 256 | 652 |
| Chi2=189.379 (0.001); Cramer's V=0.381 | ||||
Table 4 summarizes the different clinical forms of tinea observed according to patients’ gender and age group. Tinea cruris and tinea capitis were significantly more prevalent among men, whereas tinea corporis was much more associated with women. Other types of tinea did not show statistically significant associations with gender. In relation to age, statistically significant associations were found for tinea capitis and tinea corporis and the youngest age group (<16), tinea cruris and the 16–30 age group, tinea pedis and the 31–45 age group and tinea unguium and any group over 45 years.
Frequency (%) of different clinical forms of tinea according to patient gender and age group.
| Clinical form | Total | Gender | Age group (years) | |||||
|---|---|---|---|---|---|---|---|---|
| Female | Male | <16 | 16–30 | 31–45 | 46–60 | >60 | ||
| Tinea capitis | 10.6% | 7.8% | 13.1%a | 46.5%a | 0% | 0.7% | 0% | 1.7% |
| Tinea corporis | 24.7% | 30.2%a | 19.8% | 38.7%a | 28.4% | 18.5% | 23.5% | 15.1% |
| Tinea cruris | 3.8% | 1.6% | 5.8%a | 0% | 9.5%a | 4% | 3% | 5.9% |
| Tinea manuum | 2.9% | 2.3% | 3.5% | 0.7% | 4.1% | 4.6% | 3.6% | 1.7% |
| Tinea pedis | 17.5% | 18.8% | 16.3% | 6.3% | 20.3% | 25.8%a | 22.3% | 11.8% |
| Tinea unguium | 39.6% | 37.7% | 41.3% | 4.9% | 37.8% | 46.4% | 47.6%a | 62.2%a |
| No data | 0.9% | 1.6% | 0.3% | 2.8%a | 0% | 0% | 0% | 1.7% |
| Patients total N (%) | 652 | 308 (47.2%) | 344 (52.8%) | 142 (21.8%) | 74 (11.3%) | 151 (23.2%) | 166 (25.5%) | 119 (18.3%) |
| Statistical tests | Chi2=23.996 (0.001); Cramer's V=0.192 | Chi2=351.808 (0.001); Cramer's V=0.367 | ||||||
In Spain, several healthcare providers, including primary care, specialist clinicians (mainly dermatologists, but not exclusively), and emergency departments, can request diagnostic tests when there is a suspicion of superficial mycosis. In our study, 53% of the tests were requested by primary care, 32% by specialists, 12% by the Emergency department and 3% by other healthcare providers. Results highlight that 25% of skin specimens, 10% of hair ones, and 1.5% of nail scrapings were requested by the Emergency department. Emergency department also requested more tests for men than for women, and for the group of age between 16 and 30 years over the rest of the population (see Fig. 1).
Discussion
Dermatophytes distribution, as already mentioned, depends on a variety of geographic, cultural, environmental and socioeconomic factors. In Zaragoza province, rural population has decreased 7% since 1999, immigration remains a relatively recent phenomenon (in 2000, immigrants represented 1.47% of the population; today it is 12.6%) and agricultural and livestock related activities are in expansion.5
Our data point to a dramatic shift in the profile of dermatophytes over the last 35 years, where anthropophilic species, such as T. rubrum (56%) or T. tonsurans (11.3%), have conquered the arena where zoophilic species used to cause 75% of dermatophytoses.9 The local changes observed in Zaragoza Healthcare Area III are consistent with the global trends previously reported elsewhere.3,10
The promotion of sport practise in public facilities, poor hygienic standards in barbershops, nail salons and beauty cabinets, or the unprecedented mobility associated with international tourism and migratory movements may have played an active role in the global spread of anthropophilic dermatophytoses.3,10,16 In addition, COVID pandemic lockdown during 2020 might have also caused outbreaks within families due to the prolonged conviviality at home, especially in low-income settings.
Although our study lacks information on patients’ behaviour, and we can only speculate about the causes behind dermatophytoses, the demand of mycological tests has increased 53% in 4 years’ time. Furthermore, dermatophytes culture positivity rate is slightly higher (16.7%), than previously observed.9 The increased isolation may be due to higher incidence of dermatophytoses, more frequent consultation due to greater self-awareness, or to the improvement on mycological diagnostic techniques. In our setting, tinea unguium observations suggest the idea that behavioural changes within the population may be important factors that have contributed to the shift on the epidemiology of dermatophytes. Our work reports that the number of nail scrapings experienced an unprecedented dramatic increase in the period of study, whereas the profile of species causing tinea unguium has not changed in three decades.1,9T. rubrum and T. interdigitale, both anthropophilic species, are responsible for 88% of cases of tinea unguium, and nail studies represent 53% of the lab requests. As a whole, future studies should try to shed light on the reasons behind the increase of nail mycological studies in such a short time, as the identification of those reasons could help to explain better the 4:1 ratio (anthropophilic–zoophilic species) we have observed.
In our study, the most significant change in dermatophytes epidemiology involved tinea capitis, where the shift in the ratio anthropophilic-zoophilic cases is more obvious. Previous local studies9,12 showed that M. canis and T. mentagrophytes caused nearly 80% of tinea capitis cases, compared to 34% found in this study. T. tonsurans (23%) and M. audouinii (19%) have increased its prevalence compared to previous series, and Trichochyton soudanense and Trichophyton violaceum, both species associated to African immigration,1,4,6 remains a minority in our area. tinea corporis and tinea capitis show similar species distribution, except for T. rubrum, becoming one of the most prevalent dermatophytes causing tinea corporis, but not tinea capitis.
In the past, M. canis and T. mentagrophytes accounted for 52% and 31% of isolates, respectively, whereas T. rubrum accounted for just 12%.9 Nowadays, T. rubrum causes 47% of skin dermatophytoses, whereas zoophilic species are found in only 27% of the cases. It is noteworthy that the decline in the prevalence of zoophilic dermatophytes (Trichophyton verrucosum or T. mentagrophytes) coincides with the expansion of livestock-related economic activities over the past three decades. Improvement in farming conditions and animal health control in recent decades may provide a rationale for these observations. Nevertheless, M. canis remains an important dermatophytosis agent. As cats and dogs are the main source of this species, the increase of pets at home in modern urban societies, including Spanish households, may be responsible for the majority of our zoophilic infection cases. By enhancing veterinary pet control and hygienic measures at home, animal-to-human transmissions should be notably reduced.6
One of the main limitations of this work has been that recent molecular taxonomy studies have modified the concept of species in dermatophytes. As a result, a new taxonomic rearrangement has been proposed.7 Nowadays, T. rubrum species complex (T. rubrum, T. soudanense and T. violaceum)14 and T. mentagrophytes species complex (T. mentagrophytes, T. interdigitale, T. tonsurans or Trichophyton equinum, among others)13,15 are considered a set instead of individual species. The implementation of new methodology in mycology labs leads to more accurate identification data and epidemiological results, as phenotypes have proved to be poorly discriminatory. As molecular methods have not yet been broadly adopted, “traditional” epidemiological studies may be still considered a valid source of information. Thus, they can be compared to previous studies and identify changes in dermatophytes distribution, especially in low-income settings where dermatophytoses keep on being prevalent.
Finally, it should be highlighted that while dermatophytoses are a matter of concern in public health, tinea is not considered an emergency. With regard to the diagnosis of this infection, 12% of the requests at our hospital were from the Emergency department. Thus, some qualitative research should be conducted to understand better why patients seek medical attention about mild superficial lesions in the Emergency room. This would enable the design and implementation of strategies to promote tinea cases diagnoses from primary care settings instead of emergency departments.
Future research aims to explore in deep the epidemiology of onychomycosis and the comparison of geographic patterns of distribution of dermatophytes by designing a multicentric study.
FundingThis study did not receive any external funding.
Conflict of interestThe authors have no conflict of interest to declare.
The authors would like to thank S. Pablo for the statistical support and H. Powell for his assistance with the English language editing of the final version of this paper.
