Asymptomatic Scalp Carriage among Household Contacts of Children Affected by Tinea Capitis: A Prospective Study in the Metropolitan Area of Brussels, Belgium

Abstract

Introduction

Tinea capitis (TC) is a superficial fungal infection affecting the scalp. The existence of asymptomatic carriers (ACs) could represent a potential reservoir responsible of (re)contamination and failure of treatment. No prospective studies on ACs in household contacts of TC patients in Europe have been published to date.

Objectives

The aim of this study was to assess the prevalence of ACs in a cohort of household contacts of children who were diagnosed with TC in the metropolitan area of Bruxelles, Belgium.

Methods

This prospective observational study was conducted from October 2015 to April 2016 at the Dermatology Department of the University Hospitals Brugmann, Saint-Pierre, Queen Fabiola Children Hospital.

Results

Ninety-nine cases of TC from 95 different family circles were included. The main infectious agent identified was Microsporum audouinii in 53 cases. The mean age of TC patients was 5.8 years. Male/female ratio was 2.8. Eighty-one household contacts of TC patients were enrolled in the study. Two cases of ACs (5%) were identified.

Conclusions

M. audouinii was the most common pathogen identified. The prevalence of ACs we report is on average higher compared to other European large cities. Larger prospective studies including all close contacts of affected patients are required in order to establish guidelines regarding identification and management of ACs.

Introduction

Tinea capitis (TC) is a dermatophytic infection mostly affecting children [1]. Infectious pathogens vary according to geographic distribution. Microsporum canis is the most common agent identified in European laboratories, however, during the last 10 years an increase in infections by anthropophilic species has been observed [1, 2, 3, 4, 5, 6, 7, 8, 9]. The higher prevalence of total cases of TC in metropolitan areas observed in recent years could be addressed to massive migratory flows [1, 2, 7, 9, 10]. Promiscuity, poor hygiene, overpopulation, and low socio-economic status are associated with higher prevalence of TC [2]. Pre-pubertal children are most commonly affected [3, 11, 12, 13]. Spontaneous resolution in puberty is possible [3, 14]. TC represents a real public health issue, responsible of frequent outbreaks in nurseries and schools [8, 12, 15]. Alopecic patches, broken hairs, scales, pustules, kerion, and possible regional lymphadenopathy are typical clinical manifestations [11]. Atypical clinical presentations with mild or nonspecific signs make clinical diagnosis challenging. Zoophilic species are usually associated with intense inflammatory response of the host and subsequent more striking clinical presentation [1, 11]. During infection, spores spread in the environment surrounding the affected patient [11, 14, 15, 16]. Spores on the ground or in hats, brushes or combs, linings and school tools may be responsible of inter-individual transmission [1, 14, 16]. Asymptomatic carriers (ACs) are defined as individuals in which dermatophytes are identified, even though no clinical signs are observed [7, 17]. In ACs, anthropophilic species are predominant [1, 9, 18, 19]. This is explained by the fact that anthropophilic species adapt more easily to the host and induce a weaker immune response. Spontaneous resolution, development of disease, and persistence of asymptomatic carriage state for months or even years have been observed in ACs in several studies, making it impossible to predict the course of asymptomatic carriage [3, 7, 15, 17, 20]. No definitive guidelines regarding testing or management of ACs are available to date. However, addressing the issue of ACs as potential reservoir of disease could be important in order to prevent spreading and reinfection. Twenty-six studies have been published to date, with mixed results [3, 5, 7, 8, 9, 10, 15, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36]. The vast majority of them is retrospective or epidemiologic in nature. Only 2 prospective studies regarding asymptomatic carriage state among household contacts of children affected by TC have been published to date, both conducted in the USA [15, 26]. The aim of our study was to assess the prevalence of ACs in a cohort of household contacts of patients who were diagnosed with TC in the metropolitan area of Brussels, Belgium.

Patients and Methods

This prospective study was conducted at the Dermatology Department of University Hospitals Brugmann, Saint-Pierre, and Queen Fabiola Children's Hospital, Brussels, Belgium, from October 2015 to April 2016. Patients aged <14 diagnosed with TC were selected (Table 1). All cases of suspicious TC underwent scraping of scales and hair sampling from lesions using a blade or a glass slide. Family circle was defined as all persons living under the same roof of affected patients (Table 2). Family members were screened either straight after diagnosis of TC of their relative or during the 3 weeks' follow-up consultation of their relative index case. Systematic sampling of the whole scalp of the family members was performed (by a dermatologist from the Dermatology Department) using a dry swab during the consultation. This tool was preferred over others (supermarket or professional toothbrushes) as it is costless for the patients, easily available and resistant enough to allow a vigorous swabbing of all the scalp. Part of the scales was examined by incubation with potassium hydroxide (KOH) 25% and Blue Evans stain, while the remaining samples were incubated for 3–4 weeks at 27° in a Sabouraud medium containing chloramphenicol and cycloheximide. Swabs were inoculated in the medium in the same way. ACs are defined as individuals in which dermatophytes are identified, even though no clinical signs are observed. Pathogens were identified by 3 technicians experts in mycology according to macroscopic and microscopic features of the cultures.

Table 1.

Inclusion and exclusion criteria in the selection of index cases

Inclusion criteria	Exclusion criteria
Clinical signs of TC detected by a dermatologist	Absence of fungal infection at mycologic culture
Positive fungal culture only OR direct examination positive for fungal infection + positive fungal culture	Diagnosis and/or follow-up outside hospital context (i.e., private office)
Age <14 years	Incomplete patients' data in hospital registry
	Diagnosis of TC before October 2015
	Age over 14 years

TC, Tinea capitis.

Table 2.

Inclusion and exclusion criteria in the selection of the family circle (household contacts) of index cases

Inclusion criteria	Exclusion criteria
Being family member of index case living under the same roof	Presence of clinical signs of TC
No clinical signs of TC

TC, Tinea capitis.

Data such as age, sex, ethnic origin, clinical presentation, localization, results of mycological testing, history of recent travelling, presence of pets or other risk factors, treatment administered and its duration, and date of starting and ending of follow-up were collected for each patient. Negative mycological test was defined as resolution of the infection. Index cases and ACs were followed every 3 weeks, with clinical data recorder and systematic mycological sampling of the scalp performed during each follow-up visit. The subjects have given their written informed consent and the study protocol was approved by the institute's committee on human research.

Results

Over 140 TC patients selected, 41 were excluded. Twenty-one of the excluded subjects were negative at the direct examination or mycological culture; 18 were unable to undergo regular follow; for two of them, incomplete data were recorded in the hospital registry. The remaining 99 patients were enrolled in the study, of whom 73.7% were boys and 26.3% were girls. Mean age was 5.8 years, ranging from 7 months to 13 years. Ninety-one percent of affected children were younger than 10 years old. Anthropophilic species were predominant (94.9%). Microsporum audouinii was identified in 53.5% of cases of TC (shown in Fig. 1). Scaly and itchy alopecic plaques represented the most common clinical presentation. In 95 cases, TC was evoked clinically, while in 4 cases clinical suspicion was psoriasis, pityriasis amiantacea, lichen planus, and seborrheic dermatitis, respectively. On average, in 34.3% of cases, another member of the family presented clinical signs of TC and resulted positive into mycologic testing. At the end of the study, 31 over 99 patients were lost at follow-up, 11 were still undergoing treatment and 63 patients achieved resolution of infection after treatment (mean duration of treatment: 129 days). Resolution of infection from M. canis required a longer mean duration of treatment compared to infection from other pathogens (shown in Fig. 2).

Fig. 1.

Dermatophytes identified in index cases.

Fig. 2.

Mean duration of treatments according to infectious agents. M, Microsporum; T, Trichophyton.

The 99 patients affected by TC belonged to 95 different family circles. Eighty-one family members with no clinical signs of TC were screened to assess a potential state of asymptomatic carriage. Two ACs were identified (2.5%): 1 girl (AC1 − M. audouinii) and 1 boy (AC2 − Trichophyton tonsurans). Both ACs were aged <10 years. AC1 was administered oral itraconazole 5 mg/kg/day for 6 months. During this time frame, the patient never developed clinically evident lesions and swabs performed monthly still resulted positive at the end of the study. Her brother, affected by TC due to T. tonsurans, achieved resolution of infection after 1 month of treatment with oral terbinafine. Her sister, affected by TC due to M. audouinii, achieved resolution of infection after 1 month of treatment with oral itraconazole. AC2 and his brother (index case) were lost for follow-up after first consultation.

Discussion

Twenty-six studies regarding the prevalence of ACs for TC have been published to date [3, 5, 7, 8, 9, 10, 15, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36]. The majority of them were epidemiologic or retrospective studies. Only 2 investigated prevalence of ACs among household contacts of TC patients in a prospective manner [15, 26]. Both of them were conducted in the USA before 2000 and one included mainly ACs for T. tonsurans, failing to investigate asymptomatic carriage for other pathogens [30]. To our knowledge, our study is the first European prospective study on asymptomatic scalp carriage among household contacts of TC patients.

In our cohort from the metropolitan area of Brussels, the majority of TC were due to anthropophilic species (94.9%). This is in line with data from the literature [1, 2, 3, 4, 5, 9]. M. audouinii was the most common pathogen identified (53.5%). M. canis was the only zoophilic species identified, responsible of 5% of infections. Compared to the study from Kolivras et al. [9] in the same geographic area, an increase in the prevalence of anthropophilic species was observed (94.9% in 2016 compared to 89% in 2002). Such increase could be addressed to environmental factors, increase in migratory flows and to intrinsic characteristics of both pathogen and host [1, 2, 7, 9, 10, 37]. In our cohort, most patients affected by TC were aged <10 years (88.8%). Mean age was 5.8 years (7 months–13 years). This aligns with data from previous studies [2, 3, 6, 7, 8, 13, 33, 38]. White et al. [33] postulated that the higher prevalence of TC in young children could be explained by a lower content in fungistatic fatty acids in the sebum from the scalp of children compared to adults. Younger children are also most commonly exposed to close contact compared to older subjects [18, 33]. As to sex ratio, different epidemiologic studies obtained conflicting results [7, 8, 16, 31, 39]. In our series, the majority of TC patients were males (70.5%). Male predominance could be explained by the fact that boys usually have shorter haircuts compared to girls, making it easier to detect lesions on the scalp prompting medical attention [9].

Data from literature regarding prevalence of ACs vary considerably, ranging from 0.3% to 97% [3, 5, 7, 8, 18, 24, 25, 26, 30, 31, 34, 36, 38]. Prevalence varies alongside with population's features and geographic distribution, making it difficult to compare results of studies conducted in different countries and continents. In Spain and Italy where TC has been relatively rare, the prevalence of scalp carriage was 0.2% and 0.3%, respectively [15, 20, 40]. In contrast, higher prevalence rates (49%) of asymptomatic carriage have been reported in South Africa where Trichophyton violaceum TC is endemic. In the USA where T. tonsurans is prevalent, the carrier rates range from 8% to 15%. In our study, prevalence of ACs was 2.5%. No prevalence study on ACs has been conducted in Belgium to date.

Variability in the prevalence of ACs could also be the result of different testing attitude and techniques among the different studies [35]. In our series, T. tonsurans was isolated in AC1 and M. canis in AC2. Infection by T. tonsurans has been associated in other studies with higher rate of asymptomatic carriage [11, 26, 33, 35, 40].

The majority of published studies are retrospective in nature, mostly including healthy subjects from environments at risk for TC such as schools or communities. Screening of household members was performed only in a few studies. In the retrospective study on asymptomatic scalp carriage by Dessinoti et al. [7], only a minority of household contacts accepted screening. Likewise, Pomeranz et al. [15] as well as Babel and Baughman [26] failed to enroll a significant number of household members of index cases.

Although prevalence of ACs varies considerably among different studies, some found a significant number of ACs among family members of index cases, bearing potential significant impact on recurrence of disease [24, 25, 29]. Screening of all family members living under the same roof and treatment of those found positive, it is hence of paramount importance [12]. However, enrollment and screening of all household contacts can be demanding. Pomeranz et al. [15] and Babel and Baughman [26] pointed out that the majority of contacts available for screening were women, as most pediatric patients are accompanied by their mothers or grandmothers. In our series, 100% of examined household contacts were females. Despite our efforts to enroll as much family members as possible, we found particularly challenging to examine and follow-up children's fathers, as they were frequently abroad to visit their country of origin. Efforts should be made to not miss these subjects.

The optimal management of ACs is still under debate. Oral treatment with antifungals has been recommended for carriers with high spore load, while carriers with low spore load could be treated with topical treatment alone if a close follow-up is established [11]. In our series, only 1 AC (AC1) underwent treatment, as AC2 was lost at follow-up. Treatment with oral itraconazole was administered to AC1 by his dermatologist. M. adouinii was still identified at mycologic testing after 6 months of treatment; however, she never developed clinically evident lesions during the study. Of note, her siblings achieved clinical and mycologic resolution of infection after 1 month of treatment. In their family, no other AC was identified.

The small number of ACs identified represents a limitation of our study, not allowing to generalize the results. Furthermore, it was not possible to verify whether sampling modality was the same for every clinician in our study. We minimized this bias by training all clinicians enrolled in the study.

Conclusions

We add to the literature the first prospective study on TC patients and the totality of their family circle. The prevalence of ACs we report is on average higher compared to that of other European large urban cities (5% vs. 0.3%). This is probably due to higher migratory flows toward the city of Brussels. Larger prospective studies including all close contacts of affected patients are required to establish guidelines regarding identification and management of ACs for TC.

Statement of Ethics

This research was conducted ethically in accordance with the World Medical Association Declaration of Helsinki (https://www.wma.net/policies-post/wma-declaration-of-helsinki-ethical-principles-for-medical-research-involving-human-subjects/). This study protocol was reviewed and approved by the local ethical committee of the University Hospital Saint-Pierre, Brussels (No. 0.M 007) and the approval number is B076201627231. Written informed consent was obtained from participants (or their parent/legal guardian/next of kin) to participate in the study.

Conflict of Interest Statement

No conflicts of interest.

Funding Sources

No funding sources.

Author Contributions

Pauline Lecerf contributed to the conception and design of the work, data acquisition, data analysis, data interpretation, draft of the work, critical revision for important intellectual content, and final approval of the version to be published; Chantal Dangoisse contributed to data interpretation, draft of the work, critical revision for important intellectual content, and final approval of the version to be published; Aude Van Ooteghem contributed to data acquisition, draft of the work, critical revision for important intellectual content, and final approval of the version to be published; Anja Vujovic contributed to data acquisition, data analysis, draft of the work, critical revision for important intellectual content, and final approval of the version to be published; Laura Vollono contributed to data acquisition, data analysis, data interpretation, draft of the work, critical revision for important intellectual content, and final approval of the version to be published; Bertrand Richert contributed to data interpretation, draft of the work, critical revision for important intellectual content, and final approval of the version to be published. All authors agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Data Availability Statement

Data are available if required.