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Inflammatory tinea capitis: a 12â•'year study and a review of the literature

Diagnosis,Therapy and Prophylaxis of Fungal Diseases Inflammatory Tinea capitis: a 12-year study and a review of theliterature Ine s Zaraa,1,2 Abdelmohti Hawilo,1 Amina Aounallah,1 Sondes Trojjet,1 Dalenda El Euch,1Mourad Mokni1,2 and Amel Ben Osman1,21Department of Dermatology, La Rabta Hospital Tunis, Tunisia and 2University of Medicine, El Manar Faculty Tunis, Tunis, Tunisia Inflammatory Tinea capitis (TC) is a rare form of TC. The aim of this study was to reviewepidemiological, clinical and mycological profile of inflammatory TC. We present aretrospective study (1999–2010), enrolled all the cases of inflammatory TC observed ata referral hospital in the northern Tunisia. One hundred and twenty-one patients withinflammatory TC, 83 male patients (68.6%) and 38 female patients (31.4%) wereenrolled. The mean age was about 8 years. A majority of TC (71.9%) were in patientslesser than 10 years of age. Positive family history and contact with animals werenoted in seven and 35 cases respectively. Direct examination was positive in 110 cases(59 ectothrix, 51 endothrix) and positive cultures were obtained in 105 patients (49Trichophyton violaceum, 31 Microsporum canis, 13 Trichophyton interdigitale complex, 12Trichophyton verrucosum). Systemic treatment was carried out in 115 patients withgriseofulvin, in one with terbinafine. A complete recovery was noted in 88 cases; andpersistent alopecia in 28 cases. The inflammatory TC is rare, but more common inrural families. The disease mostly affected male genders (68.6%) and T. violaceumremains the common pathogen of inflammatory TC in northern Tunisia.
Key words: Kerion, Tinea capitis, dermatophytosis, Trichophyton violaceum, Microsporum canis, griseofulvin, NorthTunisia.
inflammatory reaction with sometimes devastating consequences.5–7 The true incidence and prevalence of Tinea capitis (TC) or scalp ringworm is a common inflammatory TC remain unknown in Tunisia and no dermatophyte infection of the scalp in children between large, long-term study of this form of TC has been 3 and 7 years of age.1–3 The epidemiology of TC varies conducted in recent years.
within different geographical areas throughout the The aim of our study was to review the epidemio- world.4 It may occur sporadically or epidemically, and clinical and mycological features of inflammatory TC an increase in its incidence has been noted in many diagnosed in our area and compare the pattern of countries over the last few decades. The presenting infectious agents causing inflammatory TC in our study symptoms vary widely and are mostly mild and tran- to those of previous Tunisian series and other series of sient. A more uncommon and often misdiagnosed the literature.
symptom is inflammatory TC (kerion celsi), a severe Patients and methods Correspondence: Ine s Zaraa, Department of Dermatology, La Rabta,Hospital, Jabbari, Bab Saadoun, Tunis 1007, Tunisia.
This retrospective study was performed in the Depart- Tel.: +21698307425. Fax: +21671569449.
ment of Dermatology of La Rabta Hospital of Tunis, Tunisia. We reviewed all cases of patients with anestablished diagnosis of inflammatory TC observed Submitted for publication 13 September 2011 between January 1999 and December 2010 (12 years).
Revised 6 May 2012Accepted for publication 24 May 2012 Our department is situated in the northern Tunisia. The  2012 Blackwell Verlag GmbH Mycoses, 2013, 56, 110–116

Inflammatory Tinea capitis study included all patients with clinical presentation of and 38 female patients (31.4%) with a sex ratio (M ⁄ F) inflammatory TC (suppurative and painful plaque asso- ciated with purulent drainage), which confirmed by the Our patients come from a rural region in 60 cases mycological examination (direct examination and ⁄ or (49. 59%), Tunis City in 42 cases (34.71%), and an culture positive). Mycological investigation, including a urban area surrounding Tunis city in 19 cases (15.7%).
direct microscopic mount and fungal culture, was Patients were 8.09 ± 3.99 years middle-aged (med- performed for every patient. Clinical materials (scales, ian = 6 years), [range: 18 months to 63 years]. Four hair) were examined microscopically (30% KOH solu- cases (3.3%; three girls, one boy) were diagnosed in tion). In many cases with a positive direct examination, infants less than 2 years old (ranges: 1–2 years). We the type of parasitation of the hair was also recorded.
identified six cases (4.6%) of TC in adults (more than Culture is currently required to identify the precise 18 years) among a total of 42 cases of adult TC organism. Microbiological cultures were incubated at (14.28%), concerning five men (83.33%) and one 25 C in Sabouraud 2% glucose chloramphenicol agar woman (16.67%) with an average age of 31 years and Sabouraud 2% glucose cycloheximide–chloramphe- (from 20 to 63 years). The distribution of patients nicol agar. The specimens were examined twice weekly.
according to age and sex was represented in Fig. 2. We The identification of dermatophytes was based on note that 71.9% of cases (87 cases) occurred in children the macroscopic and microscopic characteristics of the younger than 10 years of age. The mean duration fungi. For each patient, we recorded the age, the gender, of the disease prior to diagnosis was about 1.76 ± the geographical origin, duration of the disease before 1.25 months (range: 10 days to 3 years; median = consultation, the clinical presentation, the contact with other family members or with animals, the responsible Other family members were infected with tinea in dermatophyte and the evolution under treatment and seven cases and contact with animals was reported in complications. The patients were re-evaluated periodi- 35 cases (cats: 17 cases, dogs: 13 cases, rabbits: five cally for at least 6 weeks.
cases). Contributing factors were represented in threecases (2.47%): local application of corticosteroids (twocases) and gastric tumour (woman: 63 years old) in one case. None of the patients had positive HIV serology.
In clinical examination, all patients presented with Epidemiological, clinical features follicular pustular elements on squamous erythematous During the analysed period of 12 years, a total of 121 alopecic patches, realising a kerion (Fig. 3). Cervical cases (10.08 cases ⁄ year) were diagnosed with inflam- (auricular and posterior occipital) lymph nodes and matory TC among a total number of 881 cases of TC fever were found in 15 patients. Inflammatory TC was (13.73%). The year-flow for total TC was represented associated with erythema nodosum in a 5-year-old boy in Fig. 1. The incidence of TC from 1999 was (published case). Physical examination showed Tinea gradually increasing and reaching to its peak in corporis in eight cases (6.61%) (face: four cases, hand: 2006 and 2009. These are 83 male patients (68.6%) two cases, neck: one case, trunk: one case) and Figure 1 The year-flow for total inflammatory Tinea capitis and thedermatophytes isolated from the patients.
Figure 2 Distribution of patients according to age and gender.
 2012 Blackwell Verlag GmbHMycoses, 2013, 56, 110–116

I. Zaraa et al.
and rats. The annual distribution of the different speciesis presented in Fig. 1; we note a clear predominance ofT.violaceum and M. canis.
For mycological examination of inflammatory TC in adults, three cases are due to T. interdigitale complex, onecase to T. violaceum, one case to M. canis and one case wasnegative. According to our data, negative culture repre-sent 11.57% of all cultures (14 cases) and contaminatedsamples were noted in 1.65% of cases (two cases). Thesenegative cultures had a positive direct examination (10ectothrix, 4 endothrix). The relationship between directexamantion and culture is represented in Table 1. These Figure 3 Kerion of the scalp (suppurative plaque of the scalp).
results may be related to an antifungal treatmentinitiated before sampling (9.91% of our patients), because onychomycosis in five cases (4.13%). Twelve patients many antifungal drugs are retained within stratum (9.91%) were treated with an antifungal treatment corneum of epidermis for a long time and may inhibit (with too short followed schedule) before consultation.
the growth of dermatophytes on SaboraudÕs dextrose Three patients presented with a history of hospitalisa- agar or the type of dermatophyte is difficult to cultivate.
tion in surgical department with the diagnosis of The distribution of aetiological agents by gender was Staphylococcal abscess and treated by intravenous summarised in Table 2. We note a higher prevalence of antibiotics and surgical excision.
M. canis and T. interdigitale complex in male patients.
Mycological features Treatment and follow-up Direct examination was positive in 110 cases (90.9%).
Treatment regimen consisted of griseofulvin at the dose Fifty-nine patients (53.63%) were ectothrix and 51 of 20–25 mg kg)1 per day and 1 g per day in adult TC patients (46.37%) were endothrix. In the 11 cases when for 6–8 weeks for all patients except for one child direct examination was negative, the culture was (5 years old) with inflammatory TC due to M. canis, positive (Microsporum canis (four cases), Trichophyton which did not respond to systemic griseofulvin at 20 mg violaceum (three cases), Trichophyton mentagrophytes [T.
day for 4 months, was treated with oral terbinafine.
mentagrophytes is an older taxonomic name for derma- During the whole treatment period and follow-up, the tophytes belonging to the ÔTrichophyton interdigitale tolerance was excellent and no side effects or abnormal complexÕ] (three cases), Trichophyton verrucosum (one results in the blood chemistry tests were observed.
case). Positive cultures of dermatophytes were obtained A systemic antibiotic and prednisone (0.5 mg kg)1 per in 105 patients (86.77%): T violaceum (49 cases: daily) were associated with 15 cases. Antifungal topics 46.66%) was predominant, among them 13 cases of T were applied once or twice a day in all patients. The violaceum glabrum, followed by M canis (31 cases: follow-up in 116 patients (95.8%) noted a complete 29.52%), interdigitale complex (13 cases: 12.38%) and regression in 88 cases, whereas 28 showed a persistent T verrucosum (12 cases: 11.44%). Thirteen patients, alopecia. A relapse was occurred in one woman who from whom T. interdigitale complex was obtained, had a had gastric tumour. She was treated with griseofulvin history of animal contact, including rabbits, dogs, cats more than 3 months with a relapse.
Table 1 Correlation between direct examination and culture.
Mycological features  2012 Blackwell Verlag GmbH Mycoses, 2013, 56, 110–116 Inflammatory Tinea capitis Table 2 Aetiology agents of inflammatory TC according to gender.
hygiene, crowded living conditions and low socioeco-nomic status) were associated with this increased frequency.8,11,12,17 The majority of our patients come from a rural region (60 cases: 49. 59%).
Trichophyton violaceum As was found in our study, it appears most often in Microsporum canis children between 5 and 10 years of age (Fig. 2).23–25 Our results were similar to those in other Tunisian Trichophyton verrucosum studies, noting that living conditions, large family size and close contact with other infected children at school,physical contact with animals and playing outside may facilitate fungal transmission.8,11,12,26 TC, Tinea capitis.
Inflammatory TC is secondary to a vigorous host immune response and its occurrence in neonates andin infants in their first year of life is extremely infrequent and only a few cases occurring at this age We report one of the largest case series of inflammatory have been reported in the literature.27–29 The rare TC in the literature. The major findings in our study presentation of inflammatory TC at this age is probably were the increase over recent years, in the number of explained by the immaturity of their immunological cases of inflammatory TC (121cases: 13.73%), compar- system.29 In our series, we found four cases (3.3%; atively to our first study in 1998 (22 cases: 1.8%), the three girls, one boy) of inflammatory TC in infants less high incidence among boys below the age of 10 years, than 2 years old and two family members were and the rarity in adults, in which the male gender is infected with TC. The most reported factors predispos- preferred. T. violaceum was the most common pathogen ing infants to TC are humid environment, broad- in all cases and T. interdigitale complex was predomi- spectrum antibiotic use, epidermal immaturity and nantly in adult.8 impairment of health (anaemia, immunodepression).30 TC is a dermatophytosis of the scalp and hair that it We do not found predisposing factors in our infants has been a major public health problem in Tunisia for such as immunodepression or impairment of heath, decades.9 The clinical presentation is a great mimicker but they come from a rural region where hygiene and and can present itself in various ways, ranging from socioeconomic conditions are unfavourable. It has also asymptomatic carriers, scaling lesions and ⁄ or alopecia been proposed that asymptomatic carriers (mothers), to cervical lymphadenopathy and large painful inflam- without clinical signs or symptoms of TC, but with matory masses. This acute painful inflammatory boggy positive scalp cultures, could be an important source mass with alopecia on the scalp, often with crusting and of disease transmission or a reservoir of dermato- purulent discharge, is called kerion celsi and it is the result of an intense hypersensitivity reaction from a In our study, the proportion of inflammatory adult TC dermatophytic infection.10 This condition is rare, with (14.28%) is approximately in accordance with the only few articles in the literature and most of them are previous Tunisian studies (15% and 18%).14,15 The case reports.7,10–12 In our study, 121 cases of inflam- adultÕs hair seems to be relatively resistant to TC, which matory TC were reviewed between a total 881 TC may be due to protection from fungistatic free fatty acids (13.73%) and a total 96251 consultants (0.125%) in the sebum and colonisation by Pityrosporum orbicu- collected through 12 years. The prevalence data we lare.31–33 Although the rareness of inflammatory adult obtained from our study were different with results as TC could be explained by some cases of Inflammatory reported from many other regions of the world. In TC can take form of other forms of TC and treated Tunisia, the incidence of inflammatory TC is varied from precociously with favourable evolution. The most 2.3% to 13%.1,11–16 This value was lower than that reported factors for predisposing adults to TC are contact observed in Spain (18.2%) and Saudi Arabia (19.8%).17 with infected children, animals or objects, impairment of On the other hand, this rate was higher than that in health (diabetes mellitus, anaemia, immunodepression) Nepal (1.5%), Morocco (2.5%), Gabon (4%), Libya and use of topical or systemic corticosteroids.34–36 In (8.2%), China (10.3%), rural Kenya (10.1%), the United our study, one adult had used corticosteroid lotions and Kingdom and the United States.18–22 one woman had gastric tumour.
Inflammatory TC occurs predominantly in rural or The incidence of TC may also vary by gender, suburban areas and some factors (poor personal depending on the causative organism.19 This study  2012 Blackwell Verlag GmbHMycoses, 2013, 56, 110–116 I. Zaraa et al.
demonstrated that dermatophytes are more frequent in study, the direct examination was positive in 90.9% of male genders than female genders. The reason for this is the cases, while the culture in 86.7%.
not fully understood, but it indicates that gender may TC is a classic example of the changing geographical influence susceptibility to particular forms of these patterns of dermatophytosis that explain the polymor- infections. Some authors suggest that TC produced by phisms of clinical and mycological profile of TC.41,42 The M. canis are more usual in male genders, whereas there prevalence of different types of dermatophytes varies is no predominant gender for TC caused by T. violaceum, between continents and from one country to another, or that these latter may even be more common in and it is often difficult to know the precise distribution of women.17,23 However, these differences in gender have a particular dermatophyte. Some of the data from not always been noted.37 In our study, we found a Europe showed that M. canis and T. violaceum were the predominance of cases in male genders for inflamma- predominant dermatophyte in central and southern tory TC produced by both M. canis (74.1%) and by Europe.43–46 In the United States, T. tonsurans has T. violaceum (59.1%; Table 2). A possible explanation for supplanted M. audouinii and M. canis as the primary this apparent predominance in boys may be that male dermatophyte of TC.47–49 In south and central Asia, children help out on farms and have more contact with T. violaceum is the most common causative agent of TC, animals.3,23 TC can be transmitted from animals to whereas M. canis is predominated in western Asia.50,51 humans or among humans.3,20,38 In our study, only In east Asia (China), the most common species causing 28.9% patients have contacted with pets like dogs or TC was T. violaceum followed by T. verrucosum.52 The cats definitely. This lower percentage is likely due to the various organisms causing TC may present with differ- absence of systematic research of the notion of contact ent clinical patterns, which depend on the type of hair with animals in our medical records.
invasion and the degree of inflammatory host response.2 Inflammatory TC initiates as a dry tinea with scaling Inflammatory TC is most often caused by zoophilic and short hairs. Then, there is erythema and inflam- dermatophytes (M. canis, T. verrucosum and T. interdig- mation, which generating a painful lesion with clear itale complex), but also by anthropophilic (T. rubrum) borders that is covered with numerous pustules pro- and rarely by geophilic (M. gypseum) species.11,12 ducing abundant pus and may be associated with In Tunisia, a north African country, incidence and marked cervical lymphadenopathy and fever.2 All our pathogens of inflammatory TC were changed through patients presented herein had unique lesions with the years. In a study undertaken in our department typical clinical aspect of kerion and presence of lymph- between 1985 and 1998, of 22 cases of inflammatory adenopathies and fever in 15 cases. After that, the short TC, the predominant causative agents were T. interdig- hairs are gradually expelled or remain below the itale complex (40%) and M. canis (26.6%).8 During the inflammation. Finally, within around 8 weeks, cell- period of our study, M. canis was present in 29.52% of mediated immunity leads to complete elimination of the parasite. Usually, a definitive alopecia with fibrosis due On the other hand, our data showed that the to the sustained attack on the hair follicle was incidence of T. violaceum (46.6%) exceeded M. canis (29.52%). As shown in Fig. 1, the incidence of Confirmation of inflammatory TC diagnosis and T. violaceum increased gradually from 1999, peaked in appropriate treatment are therefore of particular impor- 2006, and then dropped quickly in the next 4 years. In tance in this variety. The gold standard diagnostic general, anthropophilic species tend to induce less method is fungal culture.39 This was performed in all inflammatory lesions than geophilic and zoophilic our patients. As reported in our study, some cases of ones.18 Clinic manifestation is often not very evocative; boggy kerions leading to unnecessary hospitalisations, they are not always diagnosed, allowing their release.
investigations (scanner), surgical interventions and This may be explained by the increased number of delays in diagnosis.40 The short duration of oral patients treated incorrectly before consultation. Another antifungal use may imply that patients diagnosed with explication, it is also possible that adults carry anthro- TC are still being undertreated or comply poorly with the therapy because of the inconvenient dosage and throughout life and develop inflammatory TC only if duration. If direct examination and culture are negative, immunodeficiencies or disruption of the scalp protective a biopsy should be performed and divided to perform mechanisms occurs.16 As rabbits have become domestic cultures in specific media for fungi.2 Careful examina- pets, the frequency of T. interdigitale complex has tion of people in close contact with family members as increased with higher presentation of inflammatory well as pets may help in the clinical suspicion. In our  2012 Blackwell Verlag GmbH Mycoses, 2013, 56, 110–116 Inflammatory Tinea capitis Accordingly, 13 of our inflammatory TC were produced by T. interdigitale complex and rabbits were observed in both patientsÕ environment. In the othernorth African studies (Morocco), T. mentagropytes wasthe major agent of inflammatory TC (75%).18 Inflam- matory TC is frequently caused by T. verrucosum. Cattle 1 Makni F, Ne´ji S, Sellami A et al. Les teignes du cuir chevelu are the main source of T. verrucosum infections. It was dans la re´gion de Sfax (Tunisie). J Mycol Med 2008; 18: 162– isolated in 12 cases (11.44%) in our series. Our results are different to other study in central Tunisia and 2 Rebollo N, Lo´pez-Barcenas AP, Arenas R. Tinea capitis. Actas southern Tunisia where T. verrucosum was the major Dermosifiliogr 2008; 99: 91–100.
3 Boumhil L, Hjira N, Naoui H et al. Les teignes du cuir chevelu agents of inflammatory TC.1,11,12 a lÕhoˆpital militaire dÕinstruction Mohammed V (Maroc). J Due to the high risk of scarring alopecia, the aim of Mycol Med 2010; 20: 97–100.
treatment is to achieve clinical and mycological cure as 4 Seebacher C, Bouchara JP, Mignon B. Updates on the epide- soon as possible. Special studies on the management of miology of dermatophyte infections. Mycopathologia 2008; inflammatory TC are not known. The treatment with 166: 335–52.
5 Elewski BE. Tinea capitis: a current perspective. J Am Acad griseofulvin (20 mg kg)1 per day for 6–12 weeks) has Dermatol 2000; 42: 1–20.
proven also with this type of childish TC effective.53,54 6 Isa-Isa R, Arenas R, Isa M. Inflammatory Tinea capitis: kerion, Recently, new antifungal agents (fluconazole, terbina- dermatophytic granuloma, and mycetoma. Clin Dermatol fine, itraconazole) 54 have become available to treat TC, 2010; 28: 133–6.
but did not obtained authorisation in TC in Tunisia.
7 Jaspers GJ, Werrij BG, Jagtman BA, Loza B. Severe kerion celsi due to Trichophyton mentagrophytes: a case report. Acta Pae- Fluconazole has been shown to be safe and effective diatr 2011; 100: e181–3.
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The authors have no conflicts of interest to disclose.
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Annex № 1 to the Order № February 15- "Rules of Carriage of Passengers, Baggage and Cargo" "Azerbaijan Airlines" Closed Joint Stock Company Table of contents 1. General provisions Terms, Definitions and abbreviations Compliance with laws and requirements of state authorities Electronic Ticket

Inflammatory tinea capitis: a 12â•'year study and a review of the literature

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