Scabies infection among boarding school students in Medan, Indonesia: Epidemiology, Risk Factors, and Recommended Prevention.

Introduction: Scabies has been a continuous health concern in residential institutions including boarding schools in Indonesia. The disease easily spreads in overcrowding residences. Using one of several boarding schools in Medan, Indonesia, as study site, we conducted this study to better understand the underlying factors behind scabies incidence in boarding schools. We hoped to be able to promote more effective preventive measures toward the disease. Materials and
Methods: We included all of 220 students (115 males and 105 females) in a cross-sectional descriptive analytical study, whose ages were ranging from 10 to 18 years. The diagnosis of scabies was made based on interview and physical examination. Skin scraping followed by microscopic assessment was carried out upon finding scabies-related lesion. Data on risk factors were collected using a set of pretested questionnaire and direct observation. Data were analyzed using bivariate and multivariate analysis the with Chi square and logistic regression.
Results: We found a high prevalence clinical scabies, i.e., 81 (36.8%) students, yet only one came out positive with skin scraping and microscopic examination. The factors associated with the infection were found to be younger age (odds ratio [OR]: 2.95, 95% confidence interval [CI] 0.97-6.09), sharing clothes (OR: 8.22, 95% CI 2.37-28.48), sharing bed (OR: 17.53, 95% CI 5.55-56.02), and unhygienic bedroom condition (OR: 8.18, 95% CI 3.30-20.28). Conclusions: The results imply the need for better strategies to prevent the transmission of astigmatid mites within the risky populations. We promote six recommendations for a more applicable approach toward scabies prevention in boarding schools and other institutional facilities alike. Copyright:

INTRODUCTION

Approximately 2.5% of world population suffer from scabies infestation at any point in time.[1] The prolonged pruritus due to active skin-burrowing female Sarcoptes scabiei causes debilitating itch that would lead to vigorous scratching, and therefore, superimposed bacterial infection.[2] The proportion is higher in developing nations which are lack of sanitation supporting resources.[34] However, in the more developed countries, scabies is due to overcrowding residences.[5] In Indonesia, scabies is prevalent among habitants in institutional facilities, along with pediculosis.[6] Several unpublished surveys in the city of Medan showed that the prevalence was ranging from 30% to 82% in various settings. This study was to determine the prevalence and risk factors of scabies in one of several boarding schools in Medan, Indonesia.

MATERIALS AND METHODS

Study design and population

This was a cross-sectional study, aiming to examine the prevalence and factors associated with scabies infestation in a boarding school in Medan, Indonesia. The study was conducted in June − September 2019. Subject was all 220 students in the boarding school. The map of study location is shown in Figure 1.

Figure 1

Map of the study location in the City of Medan, Indonesia

Diagnostic approach and operational definitions

Scabies

The diagnosis of scabies was based on cardinal sign found during interview and physical examination conducted by two experienced medical practitioners and a trained medical student. The cardinal sign comprised of pruritus that intensified at night, observed lesions in predilection sites, such as interdigital, wrist, elbow, axilla, thorax, back, buttock, abdomen, inguinal, feet, or scalp, living with other people with the same condition, and finding mites thru microscopic examination. Primary lesions could be nodules, papules, macules, vesicles, crusted papules, pustules, and/or excoriations. Upon finding the lesions, skin scrapings were carried out after obtaining informed consent from the students and the caretakers/guardians. The scrapings were taken from three different sites of primary, active lesion from each subject. The samples were examined microscopically in Parasitology Lab in Universitas Sumatera Utara, verified by a parasitology expert. If two of the four signs presented during the data collection, the subject would be diagnosed with scabies. Disagreement between physicians were reconciled thru discussion and revisiting the clinical manifestation.

Risk factors

Risk factors included gender, age, knowledge on prevention, bathing habit, clothing habit, sleeping arrangement, and bedroom condition. Personal hygiene behavior was examined using a validated questionnaire. Bathing habit was categorized “good” if the student took bath at least twice a day (one in the morning and one in the afternoon after daily activity or before bed), and used body soap. Clothing habit was taken as “good” if the student washed clothes with detergent, stored clothes in personal cupboard/confinement separated from other roommates and did not share clothes with other students. Sleeping arrangement was classified “good” if the student slept in personal bed, used personal linen, separated from and did not share beds and linens with other people. Bedroom condition was determined based on direct observation and scored checklist, including ventilation, light, humidity, ample sleeping space (minimum 2 m2 per person), and clean (swept, dusted, and mopped daily). Bedroom condition was taken as “healthy” if it scored ≥75%.

Knowledge on scabies prevention was assessed using pretested questionnaire. Subject was categorized having good knowledge if he/she scored ≥75% questions on the prevention, i.e., how to maintain good personal hygiene, how to maintain good environmental sanitation, how to avoid catching skin infection from others, and how to prevent from spreading it to others.

Data analysis

The data were analyzed using SPSS statistical package for Windows version 25.0, (IBM Corp., Armonk, NY). Bivariate analysis between each of independent variables and dependent variable was examined using Chi-square. Independent variables whose P < 0.25 were included in multivariable analysis and administered to binary logistic regression using backward method to find the strength of association. Variables remained in the final model were declared predictor variables, with the strength of association (odds ratio or OR) and 95% confidence interval (CI) were reported in the result.

RESULTS

The target and study populations consisted of 220 students (115 males and 105 females), who belonged to the grade 7 up to 12 in the boarding school. The age ranged from 10 to 18 years (median = 14 years). The characteristics of the study population are presented in Table 1.

Table 1

Characteristics of study population (n=220)

Characteristics	n (%)
Gender
Male	115 (52.3)
Female	105 (47.7)
Age (year)
10-14	113 (51.4)
15-18	107 (48.6)
Presence of nocturnal pruritus
Yes	81 (36.8)
No	139 (63.2)
Presence of scabies-related lesions
Yes	81 (36.8)
No	139 (63.2)
Presence of mites in microscopic examination
Yes	1 (0.5)
No	219 (99.5)
Knowledge on scabies prevention
Bad	89 (40.5)
Good	131 (59.5)

A total of 81 (36.8%) subjects were diagnosed with clinical scabies by the presence of nocturnal pruritus and scabies-related lesions. Skin scraping was carried out to all subjects with related lesions [Figures 2 and 3]. However, only one subject came out positive by microscopic examination, thus confirmed scabies [Figure 4].

Figure 2

Scabies-related lesions in wrist

Figure 3

Scabies-related lesions in interdigital area

Figure 4

Mite found from skin scraping and observed under light microscope examination

Table 2 shows bivariate analysis of factors associated with scabies infection. Knowledge on the disease prevention was not included in logistic regression because it showed no association with scabies. In multivariate analysis [Table 3], sharing bed with other students had the strongest association with scabies infestation, followed by poorly managed clothing (not washed properly and shared with other students), poor bedroom hygienic condition, and younger age.

Table 2

Bivariate analysis of risk factors in the study population (n=220)

Variables	Scabies		P	OR	95% CI
	Yes, n (%)	No, n (%)
Gender
Male	53 (46.1)	62 (53.9)	0.03*	2.35	1.33-4.15
Female	28 (26.7)	77 (73.3)		1
Age (year)
10-14	55 (48.7)	58 (51.3)	<0.001*	2.95	1.66-5.25
15-18	26 (24.3)	81 (75.7)		1
Knowledge
Bad	39 (43.8)	50 (56.2)	0.47	1.24	0.70-2.18
Good	42 (32.1)	89 (67.9)		1
Bathing habit
Poor	39 (70.9)	16 (29.1)	<0.01*	7.14	3.62-14.08
Good	42 (25.5)	123 (74.5)		1
Clothing habit
Poor	35 (81.4)	8 (18.6)	<0.01*	12.46	5.39-28.81
Good	46 (26)	131 (74)		1
Sleeping arrangement
Poor	76 (67.9)	36 (32.1)	<0.001*	43.49	16.30-
Good	5 (4.6)	103 (95.4)		1	116.02
Bedroom condition
Poor	67 (74.4)	23 (25.6)	<0.001*	24.14	11.64-50.05
Healthy	14 (10.8)	116 (63.2)		1

*P<0.25, significant to include into multivariate analysis. OR: Odds ratio, CI: Confidence interval

Table 3

Multivariate analysis of risk factors in the study population (n=220)

Variables	Coefficient	P	AOR	95% CI
Age (year)
10-14	0.886	0.059	2.95	0.97-6.09
15-18			1
Clothing habit
Poor	2.106	0.01*	8.22	2.37-28.48
Good			1
Sleeping arrangement
Poor	2.870	<0.001*	17.53	5.55-56.02
Good			1
Bedroom condition
Poor	2.102	<0.001*	8.18	3.30-20.28
Healthy			1
Constant	−4.450

Scabies=−4.450 + 0.886 age + 2.106 clothing habit + 2.870 sleeping arrangement + 2.102 bedroom condition. AOR: Adjusted odds ratio, CI: Confidence interval

DISCUSSION

Prevalence and risk factors

The study was conducted in one of several boarding schools in Medan, the capital city of North Sumatera Province, thus urban area. The students were dominantly coming from adjacent municipals in the same province. Students were living in dormitory consisted of many bedrooms. There were 10–15 people living in each bedroom, depending on the square meter. All students slept on mattresses placed on the hard floor (mostly tiles). The mattresses would be stored upright against the wall or piled up during the day to make room for day activity, and set during the night for sleeping. Sometimes, the students would put together just enough mattresses for everyone to sleep together. The students admitted that this sort of sleeping arrangement enabled the spread of infection among them. If someone in the room contracted with some contagious disease, it would be easy for the other occupants to catch the same infection, including scabies. Moreover, sometimes, occupants from one bedroom move to another room to sleepover with other friends. This would enable the wider spread of any contagious disease in the dormitory.

The prevalence of scabies in this study was based on clinical findings – thus clinical scabies – was 36.8%. With it, all subjects diagnosed with scabies must have had at least two of four criteria in the cardinal sign set in the operational definition. In this study, we found that all subjects who had nocturnal pruritus also had scabies-related lesions, as shown in Figures 2 and 3. Moreover, since all of them lived together, they have ticked three out of four criteria. We did not report the types of the lesion because they were all relatively homogenous, i.e., erythematous papules, few had excoriations due to scratching. None of our subjects had crusted scabies. This suggested that our subjects had classic scabies that was associated with a relatively low mite burden (10–15 mites infested the skin).[5]

Our study prevalence is slightly lower than the rates found in similar studies in Indonesia.[67] The skin scraping showed even smaller proportion, i.e., only one out of the 81 clinically diagnosed subjects gave positive result thru microscopic examination, thus confirmed scabies. This confirmed what was found in previous studies that although the finding of the mite microscopically from skin scrapings can prove the diagnosis, it is insensitive, invasive, and impractical.[89] Molecular test has shown different sensitivities in various studies, ranging from 37.9% to 86%.[101112] Although PCR might increase positivity, since it is costly, it is mostly suggested in pool sampling where an outbreak is suspected.[12]

In the absence of practical reference test, physicians must rely on the ability to recognize the clinical presentation.[13] Nevertheless, in some skin conditions, for example, scabies with impetigo, eczema, or other complicated scabies, it will be more difficult to differentiate scabies from other skin diseases.[914]

Male and younger students were likely to be more prone to infection than female and older students. This might have been attributed to behavioral factors rather than biological. Men attend less to their appearance and cleanliness compared to women; therefore, they are likely to be more exposed to infestation.[15] The same thing applies to the younger students versus older ones. Our study found quite similar result with a community-based study with much bigger subject conducted in Southern Ethiopia, in which children ≤15 years of age were more than two times more likely to develop scabies than those who were older.[16] However, unlike that study, we did not include children under the age of 10 years since boarding schools in Indonesia were only conducted for grades 7–12 or equal with junior and senior high schools.

In bivariate analysis, bathing habit had significant relationship with the occurrence of scabies (P < 0.05). However, in multivariate analysis, this variable did not contribute to the infestation. In this study, we discriminated participants who took bath at least twice a day from those who did less. In other studies, in Africa where sanitary facilities and culture did not encourage daily bathing, the category was more loosen up (taking bath weekly versus rarely).[17] Therefore, they found a strong relationship with the dependent variable. Since Indonesia is a tropical region with high humidity, people tend to take bath at least once a day, usually twice.

Sleeping arrangement and clothing habit were found to be the two most prominent predictors toward scabies infestation. Although students were self-provided with personal mattress, there were more than 50% that still liked to share bed with other roommates, or even with friends from neighboring rooms. The same way happened to the habit of sharing clothes, although the proportion was much less (19.5%). Students admit that they liked to share clothes because they were of the same body size. Some had to do it because they ran out of clean clothes. Sharing bed contributed to 17.53 times more to scabies infestation compared to otherwise. This result was relatively similar with another study in Ethiopia,[16] but much stronger than in another one in Uganda (OR: 2.11, 95% CI: 1.42–3.14).[3]

Bedroom hygiene was mostly well maintained (59%). However, our study found that poorly maintained bedroom was likely to be 8.81 times more related to scabies infestation than otherwise. The definition of healthy bedroom is having enough ventilation, natural sunlight, ample sleeping space, and cleaned regularly. S. scabiei is an obligate parasite, meaning that the mite needs to lodge in the host's body in order to live. An experiment showed that when detached from the host, it survived 24–36 h at room temperature with 40%–80% humidity.[18] The lower the humidity and the higher the temperature, the more difficult the mite to survive. Therefore, it is important to keep the room airy, well ventilated, and filled with natural sunlight during the day. Drying the mattress and washing the linens regularly will also help to provide unfavourable environment for the mite, thus shorten its lifespan outside the hosts.

Interestingly, we found scabies infestation was not associated with the level of students’ knowledge on the disease prevention. Most students (59.5%) possessed good knowledge, yet they did not practice accordingly. Students realized that in order to prevent this prevalent skin disease, they needed to refrain from sharing clothes and beds, yet many still did it. The gap between knowledge and practice was also demonstrated in the study from another boarding school in Indonesia.[19] We need to address this issue more seriously to propose a more strategic approach to prevent this disease from spreading in the community, particularly among the vulnerable and risky population like boarding school students.

Recommendations on disease prevention

We would like to suggest six recommendations to prevent the continuous occurrence of scabies in boarding schools and other facilities alike. First, boarding schools need to limit the density of the dormitory habitants. We are aware that most boarding schools in Indonesia face the same condition on the occupant density, and this is not an easy problem to fix, considering most of these institutions are private and affordable. However, schools need to understand that residents should be able to have ample space between them, therefore have enough distance from each bed. Arranging sleeping in bunk beds would be an option if the space is limited.

Second, there should be regular health examination, especially on some of the most contagious diseases in boarding schools, for example, skin infections, head lice, and pulmonary infections. It is important to identify the infection early on, which brings us to the third recommendation. A popular experiment by Mellanby showed that early stage of infection in a firstly infested person would be negligible for the first month.[20] Symptoms would be progressively worst after approximately 6 weeks, in which patient would suffer itching that intensifies at night, then become almost unbearable after 10 weeks. Unfortunately, within this symptomless period, female mites have already burrowed the skin and deposited eggs inside the burrows. This gap between pathogenesis and symptoms indicates how much time is wasted. Regular attention to students’ slightest symptoms should be able to prevent further development and disease transmission within this risky population. Moreover, a sensitized person would develop symptoms and lesions much rapidly, even within 24 h.[1420] Treatment could be performed faster if the disease is noticed earlier, which brings us to recommendation number four.

Five percent permethrin topical cream is the drug of choice for scabies due to its tolerance and low toxicity.[1421] The cream is applied all over the body for 12 h before washed off. Application is repeated after a 1-week time interval. All contacts – in this case roommates – should be treated simultaneously. Caretakers or school's nurses must supervise the treatment to ensure safety and correct use, as incorrect use of scabicides would trigger resistance or toxicity.

Next recommendation is isolation. Students diagnosed with scabies must be isolated in separate room to avoid contact and further transmission to other students. All beddings and clothing must be machine washed in 50°C water, or soaked in boiling water before hand washed, mattresses dried under the sun, and room cleaned thoroughly with disinfectant. We recommend the use of hand gloves when handling patients’ clothes, mattresses, and linens.

Finally, health education needs to be continuously implemented to raise awareness toward this infection. Although this study found no correlation between knowledge on disease prevention and the scabies incidence, other studies with similar populations proved otherwise.[2223] Boarding school students, as well as other high-risk populations, need to be exposed with the knowledge on regular basis. One strategy is involving schoolmates who have suffered from scabies to share their first-hand experience. Eventually, proper education will hopefully raise awareness and increase students’ practice toward disease prevention.

CONCLUSIONS

The prevalence of scabies in one of the boarding schools in Medan was still high. The factors contributing to the infestations included sharing bed or linens, sharing clothes, unhealthy bedroom condition, and younger age. We need to implement a more strategic approach to prevent the disease from continuously spreading in the community, especially those who live in overcrowding space.

Ethical clearance

Ethical clearance was obtained from Ethical Review Board of Universitas Sumatera Utara (approval number 305/UN5.2.1.2/SPB/2019). Written approval to conduct the research in the study location was obtained from the boarding school; however, we opted not to reveal the name of the school for ethical purpose. Written informed consent was given by the students and caretakers/guardians to conduct the interview and skin examination. Another written consent was needed before we carried out skin scrapings to students who were diagnosed clinically with scabies.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.