Tinea capitis: epidemiological and ecological aspects of cases observed from 1983 to 2003 in the Botucatu Medical School, state of São Paulo-Brazil

Abstracts

FUNDAMENTOS: Tinea capitis é importante infecção fúngica de interesse dermatológico e pediátrico. No Brasil sua prevalência é desconhecida, e os agentes causais principais são o Trichophyton tonsurans nas regiões Norte-Nordeste e o Microsporum canis no Sul-Sudeste do país. Conhecimento sobre gênero e espécies mais prevalentes tem importância sanitária e terapêutica. OBJETIVOS: Identificar espécies de dermatófitos, causa de Tinea capitis, em serviço universitário que atende clientela do Sistema Único de Saúde, de procedência urbana e rural, no interior do Estado de São Paulo. MÉTODOS: Amostras de casos clínicos suspeitos de Tinea capitis, procedentes da área de abrangência da Faculdade de Medicina de Botucatu-Unesp, foram investigadas por exame direto e cultivo visando ao diagnóstico e isolamento do agente causal. RESULTADOS: De 1.055 suspeitas, 594 foram confirmadas por exame direto, em 364 (61,1%) isolou-se o agente: M. canis em 88,2%, seguindo-se T. tonsurans (4,7%), T. rubrum (3,3%), M. gypseum (1,9%), T. mentagrophytes (1,6%). O sexo masculino correspondeu a 55,7% dos casos, e a faixa etária entre 0-5 anos predominou com 62,6% (p < 0,05). CONCLUSÕES: A prevalência detectada do M. canis superou o esperado para a Região Sudeste do Brasil. A freqüência de 88,2% pode estar influenciada por pacientes procedentes da zona rural. Esse dado deve ser considerado quando de decisão terapêutica.

Epidemiologia; Microsporum; Tinea capitis

CLINICAL, EPIDEMIOLOGICAL, LABORATORY AND THERAPEUTIC INVESTIGATION

Tinea capitis: epidemiological and ecological aspects of cases observed from 1983 to 2003 in the Botucatu Medical School, state of São Paulo-Brazil^*

Silvio Alencar Marques^I; Rosangela Maria Pires de Camargo^II; Aline Helena Gonzáles Fares^III; Renata Mayumi Takashi^III; Hamilton Ometto Stolf^IV

^IFull Professor - Department of Dermatology and Radiation Therapy - Botucatu Medical School – Unesp - Botucatu (SP), Brazil

^IIBiologist. Responsible for the Mycology Laboratory, Department of Dermatology and Radiation Therapy - Botucatu Medical School – Unesp - Botucatu (SP), Brazil

^III6^th-year medical student - Botucatu Medical School – Unesp - Botucatu (SP), Brazil

^IVAssistant Professor, Head of the Pediatrical Dermatology Outpatient Clinic - Department of Dermatology and Radiation Therapy - Botucatu Medical School – Unesp - Botucatu (SP), Brazil

^{Mailling address}

ABSTRACT

BACKGROUND:Tinea capitis is an important fungal infection of both pediatrical and dermatological interest. In Brazil, its prevalence is unknown, and main causal agents are Trichophyton tonsurans n northern and northeastern regions and Microsporum canis in southern and southeastern regions of the country. Knowledge on the most prevalent geni and species has sanitary and therapeutical importance.

OBJECTIVE: To identify dermatophyte species causing Tinea capitis, in a University Hospital that sees patients of the Public Health System (SUS), coming from both urban and rural areas in the interior of State of São Paulo.

METHODS: Samples of clinical cases with suspicion of Tinea capitis, coming from the area under Boucatu Medical School – Unesp’s responsibility, were investigated by means of direct examination and cultivation aimed at identification and isolation of the causal agent.

RESULTS: 594 out of 1,055 suspected cases were confirmed by direct examination, in 364 (61.1%) a causal agent was isolated: M. canis in 88.2%, followed by T. tonsurans (4,7%), T. rubrum (3,3%), M. gypseum (1,9%), T. mentagrophytes Males comprised 55.7% of the cases, and the age range of 0 – 5 years was predominant with 62.6% (p < 0.05).

CONCLUSIONS:M. canis detected prevalence was above the expected for Southeast of Brazil. The frequency of 88.2% may represent an influence of patients coming from the rural areas. These data should be considered for therapeutic decisions.

Keywords: Epidemiology; Microsporum; Tinea capitis

INTRODUCTION

Tinea capitis is a specific disease of the childhood, with an evolution ranging from acute to chronic, and caused by different dermatophyte fungal species. Knowledge of the epidemiology and ecology of Tinea capitis, egarding a country or its regions, is important for the didactic and sanitary meaning of the information, because of guidance as to screening infectious foci, adoption of preventive measures and for possible infectious agent-dependent therapeutic implications. Prevalence in the general population is theoretically unknown, with reported values that go from 0.52% in Spanish school population² 2.5% in England2 and even 13%, including subclinical infections, in students from Cleveland, USA. Contagious source of Tinea capitis is variable – it can be acquired from other patients or from fomites, in the case of anthropophilic fungi; from animals when infection is caused by zoophilic fungi and, more seldom, from contact with geophilic fungi. The more prevalent infecting species undergo variations from times to times, country to country or even within the regions of a same country, which depends on environmental and ethnical factors, socioeconomical level and populational density.⁴ In Europe, different surveys have shown Microsporum canis to be the most prevailing species, particularly in Spain, Italy and Greece.⁵ Anthropophilic species predominate in certain regions of France, England and Sweden.^4-6 One of the reasons for this variability in the epidemiological profile observed in Europe could be related to the ethnical composition of the studied population, whose migratory flows coming from Sub-Saharan and Northern Africa and Caribbean contribute to changes in the profile of prevailing infecting species.^5,6 In Spain, for instance, occurrence of Tinea capitis caused by anthropophilic species, such as Trichophyton tonsurans, T. soudanense, T. violaceum and Microsporum audoinii, was shown to be statistically higher among immigrant students as compared to natives.¹ In England, T. tonsurans was the agent diagnosed in 62 to 91% of instances, depending on the studied population and statistically related to ethnical groups originating from Sub-Saharan Africa or from the Caribbean.^4,7 In the American Continent, Tinea capitis varies in prevalence of infecting agents, and is considered to be very important in terms of public health in the US.^4,8,9 There, T. tonsurans, an anthropophilic species, is largely predominant, with increasing incidence and rates that reach 88 to 95% of the isolated fungi.^4,9 Young African-american males coming from large urban centers, with age between 5 and 18 years, are the most affected, with a relative risk of acquiring Tinea capitis 29.4 times higher than general population.¹⁰T. tonsurans is also the most prevailing species in Canada, with up to 76% of the isolated species.⁴M. canis, a zoophilic species, is the predominant causal agent in the other American countries, corresponding, for instance, to 80% of the isolated in Mexico¹¹ and 60% in Argentina.¹² In Brazil, various studies, shown in chart 1, have registered a higher frequency of T. tonsurans northern and northeastern states and M. canis in southern and southeastern states.^13-21T. schoenleinii infection, which causes tinea favosa, has been shown to be quite rare in the cited regions and countries.²²

This had the goal of adding up epidemiological data on the matter, based on data obtained at the Dermatology Department at Botucatu Medical School-Unesp (Dermatology-FMB), which sees both urban and rural population coming from the interior of the State of São Paulo.

PATIENTS AND METHODS

In the period comprised between January 1984 and December 2003, data of patients seen at the Dermatology Outpatient Clinic - FMB with clinical suspicion of Tinea capitis, were gathered. Hair, trimmed hair or scale samples from the suspected damaged area were collected and sent to the Medical Mycology Laboratory at the same service. Mycological diagnosis was made by analysis of the biological specimen, treated with 20% KOH and submitted to direct microscopic examination and culture in a cloranphenicol and actidione (Mycosel^®) -containing Sabouraud dextrose medium, kept under room temperature for at least 20 days. In positive cultures, morphological features, such as color, surface and back of the colony, were observed. Micromorphological mycelium and conidia features, such as shape, arrangement, distribution and number of internal cells in the macroconidia, were examined under lactophenol cotton blue staining. Whenever necessary, microcultivation in slides or use of potato agar to stimulate sporulation were carried out to confirm genus and species. In vitro hair perforation techniques and urease biochemical assays were also used whenever necessary. Obtained data were analyzed according to relative frequency of the various dermatophyte species, in the set of cases and according to gender and age ranges of the studied cases. Chi-square test was used to verify frequency differences among the various agents, considering 5% as the significance level. Fischer’s Exact Test was used for analysis of expected frequencies lower than five.

RESULTS

During the studied period, 1,085 samples corresponding to clinical suspicions of Tinea capitis, either from children or adults, were sent to the laboratory (Figures 1 and 2). Out of these, 596 (54.9%) were confirmed by means of culture or direct microscopic inspection. In 364 samples (61.1%), cultivation of the etiologic agent was possible. The most frequent dermatophyte species was M. canis, corresponding to 88.2% of isolated species (Figures 3 and 4). M. canis was predominant in both genders, particularly in males (p < 0.05) and it the different studied age ranges, except for those cases of tinea capitis observed in adolescents and adults. T. tonsurans with 4.7% of the isolated species, was the second most frequent, followed by T. rubrum (3,3%), M. gypseum (1,9%), T. mentagrophytes (1,6%) and Trichophyton spp. (0,8%) (Table 1). The majority of cases, n=35prevailed, with 91.3% of the identified species. In this same age range, males corresponded to 58.2% of the cases (data not shown). In the whole set of patients, those in the age range of 0-5 years, n=228 (62.8%), significantly prevailed in comparison to those above 5 years of age (p < 0.05). Frequency of M. canis was higher (p < 0.05) among patients of 0-5 years of age when compared to those above 5. On the other hand, frequency of T. rubrum and T. mentagrophytes was statistically higher in those patients over 5 years of age (p < 0.05), when compared to frequencies in patients below this age range (Table 3). Patients who were over 20 years old comprised only 7 cases (1.9%), five of which were females, all related to some kind of systemic immunosuppression, particularly that associated with systemic lupus erythematosus (three cases). Agents identified in those case are decribed on table 2. Agents identified in those case are decribed on table 2. Relative frequency of M. canis increased in every five-year period since 1984, i.e., no decrease relative to T. tonsurans was observed.

DISCUSSION

The present paper identifies Tinea capitis epidemiological profile prevailing in the interior of the State of São Paulo, according to the geographical area under the responsibility of the Botucatu Medical School Hospital-Unesp, which sees patients of the Public Health System (SUS) coming from both rural and urban areas. Besides adding up information to brazilian Tinea capitis etiological profile, the importance of the obtained data and their impact reflect not only on therapeutic decision-making, but also on epidemiological and sanitary reasoning at the regional level this study belongs to. As to therapeutics, it can still be said that griseofulvin is the golden standard for the treatment of Tinea capitis.^23,24 Used ever since 1958, griseofulvin has been established as a safe and effective drug, when prescribed in doses from 20 to 25 mg per kilogram of body weight. However, not always is it well tolerated, due to possible side effects, such as headaches and gastrointestinal disturbances, or even idiosyncratic ones, such as hypersensitivity. Under such circumstances, terbinafin, itraconazol and even fluconazol are alternatives.²⁵ Nevertheless, when the option is made for a drug other than griseofulvin, reports that suggest a smaller sensitivity of M. canis to treatment with terbinafin^26,27 have to be considered, that is, when the isolated species is M. canis, decision-making regarding treatment should take into account a differentiated usage time or the possible failure in case terbinafin is the chosen drug. The same clinical reasoning applies when the infecting species is not identified, but the patient comes from a region where epidemiological evidence indicate M. canis as the prevailing organism. Itraconazole, in the dose of 5 mg per kilogram of body weight, seems to be equally effective, be the isolated fungus M. canis or T. tonsurans,²⁸ even though there may be restrictions to its use in virtue of its cost or less experience of its use in children. From the sanitary point of view, isolation of an anthropophilic or zoophilic species implies in different interventions. In Brazil, when T. tonsurans, was the isolated fungus, active search among relatives and others coexisting under the same roof as the reference case showed rates up to 18.8% of subclinical infection, consequently the state of a healthy bearer with contagious potential.²⁹ These considerations point towards the great clinical and sanitary importance of routine etiologic diagnosis is cases of clinical suspicion of tinea capitis.

In the present study, a large predominance of M. canis, was identified, repeating, in a larger scale, findings from other institutions in southern and southeastern regions of the country. The number obtained here may have been influenced by a possible demand from rural areas, which are characteristic of this institution, even though patient provenance was not an object of this investigation. M. canis was predominant, particularly among males and in the age range of 0-5 years of age (Tables 1-3), revealing the intimate contact these children have with pets, potential infecting sources.³⁰ In adult patients, despite the low number of cases, T. rubrum was the most common causal agent, as if indicating an underlying state of systemic immunosuppression. The reason why T. tonsurans predominates in northern and northeastern states of the country is likewise not clear, having it been suggested to be adapted to the environmental conditions of those regions.¹⁶ However, one should recognize the climatic variability that exists among those regions and even within regions of a single state, which suggests that this environmental component is not the determining reason. In the U.S., prevalence of T. tonsurans is equally highlighted and is correlated to the African-American community of great urban centers, coexisting in conditions of high domiciliary family density and a socioeconomical level that is lower that country average.^9,10 The same is observed in France, the United Kingdom and Sweden (Stockholm).^4-7 The nearest reference is that of the city of São Paulo, where T. tonsurans has a prevalence of up to 31.2%,^18,19 which indicates and corroborates the theory that advocates interference of high populational densities and presence of immigrant populations in the epidemiological profile of tinea capitis.

CONCLUSIONS

A large predominance of Microsporum canis (88.2%) was identified among 364 isolates of tinea capitis at the Department of Dermatology at Botucatu Medical School-Unesp, an institution that traditionally has an important demand from patients coming from the rural areas. Predominance of M. canis was expressive, independent of gender, increasing in five-year periods considered between 1984 and 2003, period under study. Frequency of Trichophyton tonsurans (4,7%) was far lower than expected, even for the Southeastern region of Brazil, but may express the current epidemiological reality of tinea capitis in the interior of the State of São Paulo, data that should be confirmed by similar studies at other institutions.

ACKNOWLEDGMENTS

We thank Professor of Statistics José Eduardo Corrente, from the Research Support Group (Grupo de Suporte à Pesquisa – GAP), at Botucatu Medical School-Unesp, for a critical review of the paper.

REFERENCES

Received on April 15, 2005.

Approved by the Editorial Council and accepted for publication on October 11, 2005.

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*

Work done at Faculdade de Medicina da Universidade Estadual Paulista (Unesp) - Botucatu (SP), Brazil.

Publication Dates

• Publication in this collection
  16 Mar 2006
• Date of issue
  Dec 2005

History

• Accepted
  11 Oct 2005
• Received
  15 Apr 2005