Since 2006, more than 60,000 people illegally emigrated from Africa to Israel through the border with Egypt. Most of the refugees came from Eritrea, while others arrived from the Republic of Sudan and other African countries. This phenomenon has increased considerably between 2007 and the end of 2012. A significant portion of this population has settled in the southern Tel Aviv area. As mentioned, this population, generally of a low socioeconomic status and residing in dense living conditions, and less likely to visit a tertiary clinic with expert dermatology services, is susceptible to Tinea capitis epidemics. Due to a focal outbreak of Tinea capitis among children of refugees from Africa that immigrated to Israel, and in order to prevent epidemics and in other communities, this work attempted to characterize the clinical manifestations and provide primary physicians with appropriate diagnostic and management guidelines, to minimize the need for referral to dermatology services.
In accordance with the literature, and as shown in Fig. 3a, T. violaceum was the most common cause of Tinea capitis, in refugee children as in refugee in the US, Europe and Israel of African descent [5, 8, 16–17]. Furthermore, 75% of positive cultures showed that the source of infection was an anthropophilic fungus, strengthening the conclusion that patients infect each other at day care facilities and at home, due to the dense living conditions and lack of sufficient hygiene.
The most common clinical finding in children with either positive culture or positive direct examination was scaling, observed in 91 % and 97% respectively, aligning with a previously published report [12]. However, in contrast to this earlier report, that dealt with urban hospital-based general pediatric practice, which introduced a significantly higher chance of having a positive culture, as there are more signs on physical examination, in the present study, the majority of children with positive culture or positive direct exam had one positive sign, which was scales (53% and 48%, respectively). Moreover, the previous work found a high association between lymphadenopathy and positive Tinea capitis cultures, which stands in contrast with our results, in which only 4.7% of the children with positive culture and 7.7% of those with positive signs on direct examination, presented with lymphadenopathy. A different immune response to the same infection may underlie these conflicting observations, which would require adoption a different approach right from the start.
In the current study population, many parents who visited a dermatologist with their infected child stopped the follow up at various stages, some even after only one visit, due to long queues, distant clinics, loss of workdays and more. Some of the parents returned to the dermatologist only because the teacher refused to take the child back to the day care center until he healed or due to development of infection and fever, as in cases of kerion, which necessitated a visit to the dermatologist. Thus, treatment should be given to ensure suitable and efficient management from the initial and possibly only encounter with the patient.
In previously reported cases of Tinea capitis, insufficient response of tinea capitis in skin of the color population to treatment was not solely due to lack of compliance, but rather, to a reduced clinical response of the fungi to the conventional griseofulvin doses [15]. As a result, over the past few decades, dosage elevations have been necessary to achieve clearance. This might be due to suboptimal absorption of the drugs, different host response patterns to the same fungi or evolution of resistance of the fungi to the drugs [15].
No specific association was observed between eosinophilia or IgE levels and susceptibility to Tinea capitis infection. However, this lack of correlation may have been the result of the small sample size, or maybe because systemic signs in these children are subtle when compared to the regular pediatric population, that can be pertained to a different immunologic response of this population to fungi or parasites expect in cases of Kerion.
The four children who had no clinical response to griseofulvin, turned out to have a Rhodotorula mucilaginosa-positive culture. Although rare, in particular in immunocompetent patients, scalp infection due to these unicellular pigmented yeasts that mimic Tinea capitis, has been observed in refugee population before [18]. Several therapeutic approaches have been described, including amphotericin B, ketoconazole, fluconazole, itraconazole and flucytosine, however, there is no consensus on the preferred treatment for such infections [18].
For a refugee patient, considered a part of a high-risk population, a full physical examination should be performed. If findings like scaling, alopecia or pruritis are identified, the physician must rely on his clinical index of suspicion and should treat in accordance with the highest degree of suspicion, by providing empirical treatment, from the first encounter [19], as culture results may only be provided after 2–4 weeks and advanced test, such as PCR, may not be available in most outpatient clinics. Prescriptions for the entire treatment period should be given in advance, because it might be the only encounter with the patient.
Despite the challenges of follow up in this population, and in accordance with the literature, in any case of suspected Tinea capitis, the scalp should be cultured prior to treatment [2], at least for epidemiological investigation. If opportunity arises, follow-up with a repeat mycology culture is recommended at the end of treatment as a definitive diagnosis of eradication [1].
Due to the relative resistance to traditional dosages of griseofulvin observed in this population and failure to regularly follow up, these patients should be treated at a higher dosage than usual. Although treatment decisions rely on the identity of the fungus [14, 19–20], griseofulvin at a dosage of up to 50 mg/kg/day is recommended for first-line treatment, since it provides a sufficient clinical response. In addition, years of experience with the drug have demonstrated its long-term safety13; it has the fewest known drug interactions [15], a favorable adverse-effect profile21 and rarely induces serious adverse-reactions [2]. Griseofulvin treatment has been associated with a small number of minor adverse effects mainly gastrointestinal symptoms (vomiting, abdominal pain, diarrhea). Furthermore, it is the cheapest antifungal drug [13], a critical criterion in the population of interest, for maintaining long-term compliance. When considering these benefits against the potential damage, empiric treatment prior to culture results is recommended [22]. As shown in Table 4, the study population seemed to be resistant to fluconazole. It is therefore not recommended to treat them with this drug, as it may result in lower compliance. Topical treatment alone, yielded no clinical resolution, particularly in this population, and therefore should not be given as a single treatment, but only as adjunct therapy. In case of an inflammatory lesion, such as kerion, additional treatment with steroids and antibiotic is needed. All the medications should be given together, thus increasing compliance.
Eradication is worthless in cases of cycles of reinfection. It is therefore critical that the physician attempt to establish a relationship of trust with the parents in order to achieve whole-family care. It is also recommended to sterilize all shared hygiene instruments and wash bedding frequently. There might be a need for multidisciplinary collaborations (social worker, medical specialists) so that treatment plans and appointments can be coordinated with parents, and perhaps go as far as to hold mass testing in the neighborhood/schools to hopefully eradicate this fungal infection plaguing the immigrant community and to prevent its spread to other communities.
The key aim of this study was to emphasize the importance of diagnosis and treatment of these immigrant children by their primary pediatric doctor since it takes, as mentioned, an average of 4.3 months until they visit a dermatologist. During this critical time period, the scalp can become seriously and permanently damaged, and the infection can become systemic or cause an outbreak within the entire community. In conclusion, we recommend to relate to scaly scalp in high-risk populations as tinea capitis, and to treat with griseofulvin at a dosage of up to 50 mg/kg/day, starting from the first presentation to the pediatrician.
Declarations
Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.