Tinea capitis : A tropical disease of hygienic concern among primary school children in an urban community in Nigeria

Tinea capitis is the most common dermatophyte infection in school age children in developing countries and is known to impact negatively on their health and well-being. This study determined the prevalence of T. capitis and its relationship with hygiene among primary school pupils in Ile-Ife. This descriptive cross-sectional study recruited randomly selected pupils from public and private schools in Ile-Ife from March to April 2017. The data was collected with the use of a pre–tested intervieweradministered questionnaire on hygiene followed by physical examination. Children with a clinical diagnosis of tinea capitis had scalp and hair scrapings for microscopy and culture. Data were analyzed using descriptive and inferential statistics. A total of 420 pupils participated, 240 (57.1%) males and 180 (42.9%) females aged between 4 and 16 years. The overall prevalence rate of T. Capitis infection was 21.7% with etiological agents consisting of Epidemophyton floccosum (12.0%), Microsporum gypseum (7.7%) and Trichophyton mentagrophytes (7.7%) while 33% grew Aspergillus niger (a contaminant) and no organism was isolated in 36 (39.6%) clinically diagnosed cases. The infection was prevalent among pupils sharing combs, had close contact with animals, playing with sand and lower socio-economic status. School type and personal hygiene were the major determinants of tinea capitis infection. Prevalence of T. capitis infection among school children was high and the infection is associated with poor level of hygiene and low socio-economic status. Health promotion and health education interventions are needed to promote good hygiene, early identification and treatment of the infection.


INTRODUCTION
Tinea capitis is a fungal infection of the scalp.It is an important infective superficial dermatological disease of worldwide distribution among children.The fungus is either within the hair shaft (endothrix) or spread out over *Corresponding author.E-mail: funmitoabioye@yahoo.com.
Author(s) agree that this article remain permanently open access under the terms of the Creative Commons Attribution License 4.0 International License the hair surface (ectothrix).Tinea capitis usually gives dull gray, circular patches of alopecia, scaling, itching, and often with a black dot (Brooks et al., 2010).
T. capitis is much common in children, especially those of black African origin, whose scalp and hair seems more susceptible to fungal invasion (Kumar and Clark, 2009).
In the tropics, tinea capitis is usually aesthetically unacceptable, as it "can be unsightly or disfiguring" (Fathi and Al-Samarai, 2000).In Nigeria, its prevalence has been correlated with the warm humid climate, crowded living, poor sanitary condition of majority of the populace, which has been enhancing the spread of the disease (Ayanlowo et al., 2014).
T. capitis is a not a notifiable disease in Nigeria but it is a cause for concern due to its contagious nature.It inflicts a lot of psychosocial trauma due to attached social stigma as well as representing a potential source of secondary bacterial infection if not adequately treated.It is endemic in Nigeria and many factors have been attributed to the spread of this condition which includes warm and humid conditions, poor socioeconomic status of the majority of the populace linked to poor environmental sanitary conditions (Anosike et al., 2005).
Attention is not drawn to it because of the relatively benign course of the disease and also not being a notifiable disease.Thus, the actual prevalence figures are unknown in many endemic areas (Anosike et al., 2005).Variety of treatments have been formulated by the locals and applied, majority of which are largely ineffective and has contributed to its relative persistence in this community.
Ringworm of the scalp is presently one of the commonest dermatophytoses in Nigeria.Published reports are however very scanty in this area and a major study in Ile-Ife was last conducted in 1985 (Ajao and Akintunde, 1985) which focused mainly on the prevalence of the disease and the aetiological pathogens.Other studies had also looked at prevalence without relating it to hygiene.This study however intends to assess the prevailing situation of T. capitis and its relationship with level of hygiene.

MATERIALS AND METHODS
Cross-sectional study was conducted at Ife Central local Government Area of Osun State, Nigeria among primary school pupils during the months of March and April, 2017.The minimum sample size was determined by using the formula for calculating sample size for single proportions (Araoye, 2003).ndesired sample size z -confidence level which corresponds to the standard normal deviate usually set at 1.96 p -Prevalence = 45% that is, 0.45 (Dogo et al., 2016) σ -Error margin i.e. a degree of accuracy required and usually sets at 5% that is, 0.05 n = 380 (which was rounded off to 420 to allow for attrition of 10%) A list of all the private and public primary schools in Ife central area was retrieved from the Local Inspectorate of Education office.It contained a total of 36 public schools and 20 private schools.Multistage sampling technique was employed to select the respondents.At the 1st stage, schools were stratified into private and public thereafter at the 2nd stage, 4 schools each were selected from both public and private schools from a list of schools making a total of 8 schools using a simple random sampling technique.At the 3rd stage, 210 pupils each were selected to participate from public and private schools using sampling proportionate to size based on enrolment in each school.In each of the schools, pupils from all levels were selected randomly from class list.
Pupils of public and private primary schools whose head teachers accepted to participate in the study were enrolled in the study while pupils who were ill or not willing to participate in the study were excluded.An interviewer-administered questionnaire was used to assess the pupils' personal and school hygiene.The questionnaire contained 2 sections: biodata and hygiene practices of pupils.Information on the educational status of the mother and the job description of the respondent's father was also collected and used for socioeconomic stratification into social class 1 to 5 (Oyedeji, 1985).
In this study, class 1 and 2 were grouped as upper social class, class 3 as middle social class while class 4 and 5 were grouped as lower social class to aid data analysis.Personal hygiene score was calculated by scoring individual pupil's bathing frequency, frequency of washing hair with soap, comb sharing, frequency of hair-do, playing with sand and playing with domestic animals.The scores were categorized as poor (0 to 2), average (3 to 5), good (6 to 9).The internal consistency was assessed using Cronbach's alpha and split half technique.Cronbach alpha was 0.51 which was fair and split half had equal loading.
A physical examination was also conducted to assess students for T. capitis by a public health physician who assessed the following characteristics (scaly patches on the scalp, with or without hair loss; partial hair loss with broken-off hairs, brittle and lusterless hair strands, annular lesions with fairly sharp margins, massive scaling and folliculitis).Skin scrapings from the active edge of the lesion were taken into a sterile blotting paper using the edge of a glass slide from those with features suggestive of T. capitis.Samples were thereafter taken for mycological examination.Identification of all specimens taken from the scalp were done by direct microscopy with 10% potassium hydroxide.Specimens were cultured in sabouraud dextrose agar impregnated with chlorhexidine and the samples were then inoculated into separate petri dishes  Informed consent was obtained from parents while assent was taken from the pupils.All patients with T. capitis were treated with topical antifungal agent (Whitfield's ointment, which contains 6% w/w benzoic and 3% w/w salicylic acid).

RESULTS
Table1 showed that two-fifth of the respondents (40%) were within the age group of 7 to 9 years.Majorities were of the Yoruba ethnicity (52.4%) and were in the middle social class (47.6%) while mother's highest level of education was primary school (42.9%).Table 2 showed the prevalence of T. capitis was 21.7%.Aspergillus brasiliensis a contaminant was the highest fungal isolate (33%) while Epidermophyton floccosum (12.0%) was the commonest dermatophyte isolated followed by Microsporum gypseum and Trichophyton metangrophytes (7.7%) each.
Regarding the result of Table 3, present study showed that less than half of the respondents (47.0%) had their bath twice daily, while 52.4% shared their combs with others.Majority of the respondents (51.3%) washed their hair with soap daily.Most of the female respondents had their hair done once in a month (50.0%) while 44.2% of the boys shaved with their personal clipper.About 14% of the respondents played with sand and 42.8% played with domestic pets.Overall about half of the respondents (48.6%) have poor level of hygiene.This study revealed that there was a statistically significant association between social class and presence of T. capitis with 13% of pupils from upper social class having T. capitis compared to 42% of those from lower social class (p<0.001) and a statistically significantly higher proportion of pupils from public school having T. capitis (25.7%) compared to 17.6% of pupils from private school (p=0.04).There was no statistically significant association between sex and presence of T. capitis (p=0.34) as shown in Table 4.
According to Table 5 there was a statistically significant relationship between frequency of bath and presence of T. capitis with over a third of the respondents(36.8%)who had their bath daily having T. capitis compared to 6.7% of their counterpart who had their bath more than once daily (p< 0.001).33% of respondents who shared combs had T. capitis compared to 10% of their counterparts who do not share comb (p<0.001).28% of the respondents who played with domestic animals/pets had T. capitis compared to 17% of those who do not (p<0.001)while 92% of those that played with sand had T. capitis compared to 10% of those that do not play with sand (p<0.001).There was a statistically significant relationship between upkeep of the hair in both sexes and presence of T. capitis (p<0.001).Use of personal clippers was also associated with T. capitis with T. capitis occurring in 11% of those who use personal clippers compared to 27% of those who do not use (p=0.003).
The principal determinants of T. capitis were school type and personal hygiene status.Pupils in a public school were four times more likely to have T. capitis than those in private schools.Pupils with good hygiene were four times less likely to have T. capitis than those with poor personal hygiene (Table 6).

DISCUSSION
T. capitis has been shown to be a major public health challenge in primary school pupils in Nigeria and all over the world and this has again been demonstrated in this study where the prevalence of T. capitis among primary school pupils is 21.7%.This was found to be higher when compared to a similar study done in Ile Ife by Ajao et al. (1985) with a prevalence of 14.0%, which might be suggestive of an increase in the prevalence of the disease over the years.It is also higher compared to studies by Emele and Oyeka, (2008) and Enendu and Ibe (2005) in eastern Nigeria who found a prevalence of 9.4% and 13.9% respectively which could probably be due to difference in geographical location for the study.
The prevalence of T. capitis from our study was found to be lower than that by Akinboro et al. (2011) in a community in Oshogbo among children aged 5 to 16 years with a reported prevalence at 43.5% which may not be unconnected with the fact that their study was done in the community as opposed to school based in our own study.
The present study assessed primary school pupils who were within the age range of 4 to 16 with the most being between 4 and 12 years old which is the age range purported to have the highest prevalence as reported by Akinboro et al. (2011).T. capitis is the most common type of dermatophytosis among children and most commonly spread by close contact, especially in schools and households from human carriers, pets and via inanimate objects like combs, clippers and hairdresser equipments (Akinboro et al., 2011;Chepchirchir et al., 2009).There is no demonstrable sex predilection for T. capitis in this study which is at variance with other studies (Dogo et al., 2016;David et al., 2010;Emele and Oyeka, (2008); Enendu and Ibe, 2005;Nweze, 2001).Various conflicting views exist regarding the sexual predominance of T. capitis which may be attributed to hairdressing and styling practices such as tight hair braiding, shaving of the scalp, plaiting, and the use of hair oils which may promote disease transmission.However, the precise role of such practices remains a subject for another study.
In this study, majority of respondents from lower social economic class had T. capitis.This is in keeping with findings of other studies that revealed the link between lower socio-economic status and prevalence of T. Capitis (Ayanlowo et al., 2014;Akinboro et al., 2011;Ajao et al., 1985).The findings in our study might be due to the fact that parents of children from lower socio economic status may not have enough funds to provide personal clippers, individual combs, bedding materials, and toiletries for their children and this can result in easy spread of infection among such children once one of them is infected from school or in the neighbourhood.Such children may also live in slums with poor environmental hygiene and overcrowding which facilitate growth of the organism.
Children from low socio-economic class may not access care on time due to lack of funds or ignorance on the part of their parents.This study showed that there was higher prevalence of T. capitis in the public schools compared to the private schools.This was similar to finding from a comparative study of T. capitis in children of public and private schools in Rivers state, Nigeria (Wokoma, 2009).This may be due to the fact that children of lower social class are more likely to attend public schools where little or no school fees is paid and lower social socio-economic status have been found to be responsible for higher prevalence of the disease in this study and also buttresses the influence of seasonality and geography on skin diseases.
The predominant fungal isolate in this study was Aspergillus niger (33%) which was contrary to the findings of other studies (Akinboro et al., 2011;Enendu and Ibe, 2005;Ayanbimpe et al., 2003;Ajao and Akintunde, 1985) and this could be as a result of climatic influence on aetiology of mycoses.Epidermophyton floccosum (12.2%),M. gypseum and T. metangrophytes (7.7%) were the least isolated organisms.The findings from this study revealed that T. capitis was more among those that bath daily compared to those who bath more than once daily.This may be because most houses do not have pipe-borne water therefore some children have to trek some distance to access water, some of whom on their way to get water play with sand, carry buckets on their heads and may have contact with the infectious agents.This lack of easy access to water may reduce frequency of bathing and allow colonization of the skin by the fungi agents following contact with the infectious agents.There was higher prevalence of T. capitis in those who had close contact with pets or domestic animal compared to their counterparts in this study.This was similar to findings from a study from Sokoto state of Nigeria where livestock and pet domestication was found as a common practice in households.That study established the fact that domestic animals are important reservoir of tinea (Ameh and Okolo, 2004).Other studies have also shown that children having close contact with animals or pets had T. capitis compared to their counterparts who do not (Ayanlowo et al., 2014;Ginter-Hanselmayer et al., 2007).It is culturally believed in this environment that rearing animal can prevent evil from occurring in a household, households also rear animals for sale and personal consumption.Some of these animals habour fungi infections and children have close contacts with such animals which might explain the reasons for more T. Capitis infection among those in close contact with pets and animals compared to those who are not.This study revealed that children with proper upkeep of their hair and those who possess personal clippers had less prevalence of T. capitis compared to their counterparts who do not.This is in line with findings gotten by Akinboro et al. (2011) at Osogbo andDavid et al. (2010) in Adamawa state that showed that barbing equipment can habour fungi infections and thereby transmitting it.
The findings in this study might be due to the fact that regular hair upkeep and possession of personal clippers and combs reduces exposure to the barbing and hairdresser equipments which may harbor the tinea infection.Hygiene status of an individual's skin has been cited as one of the risk factors associated with the acquisition of dermatophyte infections.The poorer the hygiene, the higher the chances of acquiring infection.This assertion is corroborated by our study which reported a statistically significant relationship between level of hygiene and presence of T. capitis.This finding is in keeping with findings of other previous study in Nigeria and other African countries (Amoran et al, 2011;Ali et al., 2009;Menan et al., 2002).

Conclusion
Prevalence of T. capitis is still high in this environment, personal hygiene and socio-economic status are important predictors of T. capitis infection.Thus, more attention needs to be paid to personal hygiene through health promotion and education interventions to reduce the scourge of T. capitis.

Table 1 .
Socio-demographic characteristics of respondents.Ethical clearance was obtained from the Ethics committee of the Institute of Public Health, Obafemi Awolowo University, Ile-Ife (HREC number: IPHOAU/12/657).Permission was taken from the Local Inspectorate of Education office and school authorities.

Table 2 .
Frequency of culture isolates of T. capitis in studied group.

Table 4 .
Association of T. capitis with some socio-demographic characteristics.