Prevalence of scabies and impetigo in the Solomon Islands: a school survey

Background Scabies, a parasitic disease of the skin, is a major public health problem, largely affecting children. Scabies is often complicated by impetigo which can result in serious complications including invasive infections and immune mediated diseases. Scabies and impetigo are reported to have high prevalence in tropical settings including the Solomon Islands. Methods We conducted a cross-sectional prevalence survey at Gizo Primary School in the Western Province of the Solomon Islands in August 2018. The diagnosis of scabies was based on criteria developed by the International Alliance for the Control of Scabies in 2018. Population attributable risk was calculated to determine the effect of scabies on the prevalence of impetigo, and both adjusted and unadjusted risk ratios were calculated to identify differences between sexes and age groups. Results A total of 324 students were assessed (47.5% of those enrolled at the school). The prevalence of scabies was 54.3% (95% confidence interval [CI] 48.7–59.8) and most disease was mild (68.8%). The prevalence was higher in males (63.5%; adjusted risk ratio [ARR] 1.4, 95% CI 1.1–1.7), and in those aged 10–12 years (61.4%; ARR 1.8, 95% CI 1.1–2.9 when compared to those aged 4–6 years). The prevalence of impetigo was 32.1%, with males more likely to be affected (41.7%, ARR 1.7, 95% CI 1.2–2.4) but with no significant differences between age groups. 63.5% of those with impetigo had scabies, corresponding to a population attributable risk of 11.8%. Conclusions There is a very high burden of scabies and impetigo among primary school students in Gizo. There is a critical need for the development and implementation of control programs in areas where scabies is endemic.


Background
Sarcoptes scabiei var. hominis is a parasitic mite that burrows into human skin. Infestation with the mite results in an inflammatory reaction producing skin lesions with severe pruritus. Persistent scratching results in broken skin, compromising its barrier function and facilitating secondary bacterial infection with group A Streptococcus (GAS; Streptococcus pyogenes) or with Staphylococcus aureus, presenting as impetigo. Impetigo may progress to severe skin and soft tissue infection, bone and joint infection, sepsis or the immunemediated complications of GAS infection such as glomerulonephritis and potentially rheumatic fever [1,2]. Although a range of effective treatment options for scabies exists, the highly contagious nature of the disease makes its public health control challenging.
Scabies is estimated to affect more than 200 million people, especially children [3,4]. Despite these estimates, a major barrier for global disease control is the scarcity of epidemiologic data [5,6]. Prevalence surveys using systematic and standardized methods are likely to be a crucial component in determining the global burden of disease and identifying areas where the disease is endemic. The International Alliance for the Control of Scabies (IACS) undertook a Delphi study in order to establish consensus diagnostic criteria for scabies [7]. The 2018 IACS Criteria provide standardized diagnostic methods to enable evaluation and comparison of global prevalence data.
Schools have been a focus for both surveillance and control of neglected tropical diseases (NTDs), including schistosomiasis and soil-transmitted helminthiases [8]. School screening studies conducted in Africa and Asia have investigated the burden of scabies, either in isolation, or in conjunction with other NTDs or skin conditions [9,10] but there have been no school-based studies from the Solomon Islands. Locally relevant epidemiological evidence of the burden of scabies is required for the design and implementation of community scabies control programs. The primary objective of this study was therefore to determine the prevalence of scabies and impetigo in the population examined using a school screening method. The secondary objectives were to investigate features associated with scabies and impetigo. We also aimed to describe the severity of scabies and impetigo and the distribution of scabies cases using the 2018 IACS Criteria subcategories.

Study setting and participants
This was a cross-sectional, school-based study that took place in the public primary school in the town of Gizo, the capital of the Western Province of the Solomon Islands. The population in the Gizo region is approximately 7000 [11]. The setting was selected because it is the site of a planned trial. The school was selected as the study site because of the simple facilitation of recruitment of participants within a school setting and its convenient location within the centre of the town.
At the commencement of 2018, the primary school had a school roll of 682 students, consisting of students residing in Gizo town and those who travel by truck or boat from surrounding villages or islands. Students at the primary school are aged 4 to 15 years, with class groupings based on aptitude rather than age.

Study procedures
All students attending Gizo Primary School were eligible for inclusion in the study. All patients underwent a standardized examination for scabies and impetigo.
Clinical assessment was performed by doctors with expertise in scabies diagnosis, and by nurses with clinical experience in scabies diagnosis, supplemented by a training program on the diagnosis of scabies, impetigo and other locally common skin conditions. Scabies was diagnosed using the 2018 IACS Criteria [7]. Although eight subcategories exist in the IACS Criteria, only four were relevant for diagnosis in this study (Table 1). Subcategories of diagnosis that required specialized equipment (including microscopy and dermoscopy) or required examination of the genitals, were not used, as these were not practical for a field survey in this context. Impetigo was diagnosed on the presence of papules, pustules or ulcerative lesions with associated erythema, crusting or pus. Skin examination consisted of assessment of exposed areas: the feet and legs to the thighs, hands to the upper arms, neck, face and scalp. Students were in school uniform which consisted of above-knee shorts and above-elbow shirts or dresses. Shoes were removed prior to examination. A focused history of standardized questions was taken of all participants with skin lesions consisting of information required for the IACS Criteria classification. Questions included whether participants experienced itch. Contact history was assessed by asking if participants lived with someone, or had a friend or classmate with itch, or if they lived with someone, or had a friend or classmate with a rash that looks like scabies. Participants were shown images of people with typical scabies rashes to assist these questions. History was taken in the local language (Solomon Islands Pijin). Permethrin was supplied for individuals diagnosed with scabies. Permethrin was also supplied for household contacts of diagnosed children, as per local treatment protocol. No treatment was supplied to examined children without scabies. If other conditions were diagnosed, referral was provided to the local health clinic.

Data collection and statistical methods
Demographic information was collected including participant age, sex and school grade. Scabies diagnosis was classified into one of three IACS Criteria subcategories (Table 1).
Following methods used in previous studies, severity of scabies and impetigo was assessed based on the number of lesions present [12,13]. Scabies was categorized as: mild, 1 to 10 lesions; moderate, 11 to 49 lesions; or severe, 50 or more lesions. Impetigo was classified as: very mild, 1 to 5 lesions; mild, 6 to 10 lesions; moderate, 11 to 49 lesions; or severe, 50 or more lesions.
Prevalence for scabies and impetigo was calculated for each demographic group. Risk ratios were calculated using generalized linear models, adjusting for age group and sex. Population attributable risk was calculated to further analyze association between scabies and impetigo [14].
Data were collected on forms during the study period and then transcribed and uploaded to a REDCap study database (Research Electronic Data Capture), hosted at Murdoch Children's Research Institute [15]. All statistical analysis was performed using Stata (version 15, Sta-taCorp, College Station, TX, USA).

Ethics statement
Parents were provided with written information regarding the study. A community information night was also held at the school where members of the study team provided further information and answered questions. Written consent was obtained from parents or guardians of all participants and verbal assent from children where possible.
Ethical approval was granted by the Royal Children's Hospital Melbourne Human Research Ethics Committee (reference number 38099A) and the Solomon Islands Health Research and Ethics Review Board (reference number 05/18).

Results
Over 6 days in August 2018, 324 students were recruited and examined (47.5% of those enrolled at the school). All consenting students present at school during study days were examined. Doctors examined 247 participants (76.2%) and the remainder were examined by trained nurse examiners. Of those examined, 51.9% were female and the mean age was 9.6 years (standard deviation 2.3, range 4-15; Table 2).

History features
Itch was reported in 81.8% of individuals with scabies (n = 144) and in 18.4% of those without scabies (n = 21, missing = 34). A positive contact history was reported in 92.1% (n = 161) of those with scabies, and in 52.6% of those without scabies who were asked (n = 60, missing = 34). The most common contact history reported was having a friend or classmate with a rash that looks like scabies (75, 95%CI 67.9-81.2, Table 4). Of those with scabies, 26.1% (n = 46) reported either a history of itch or a positive contact history and 73.9% (n = 130) had both history features. Of those without scabies, 46.5% (n = 53) reported either a history of itch or a positive contact history and 12.3% (n = 14) had both features.

IACS criteria
The majority of scabies cases (n = 128, 72.7%) were classified as Clinical Scabies, subcategory B3, with typical clinical features, itch and contact history according to the IACS Criteria (Table 3). Only four individuals (2.3%) were identified to have clinically visible burrows (B1).

Discussion
Our study highlights the very high prevalence of scabies (54%) and impetigo (32%) in school-aged children in Gizo. The prevalence of scabies is higher than a previous study conducted in the same region in 2014 which reported a prevalence of 23% in children aged 5 to 14 [12]. High scabies prevalence has been described in other disadvantaged populations including in children in Fiji (55.7%) [13], rural communities in Nigeria (65%) [16] and amongst asylum seekers in the Netherlands (33.5%) [17].
In our study, males were more likely than females to have scabies, which has been reported previously [18,19], although this finding is not represented in the Global Burden of Disease Study (2015) estimates [20].
The majority of scabies seen was classified as Clinical Scabies according to the 2018 IACS Criteria (Fig. 2). This was consistent for males and females. Very few scabies cases (4%) had either atypical lesions or an atypical distribution of their rash. We found that the 2018 IACS Criteria for the diagnosis of scabies were easily integrated and implemented into our study design.  Implementation of these criteria in other settings would allow comparison across studies and regions. The high prevalence of impetigo (32%) is consistent with other studies from Pacific Island nations, including in Fiji (26%) and a previous study in the Solomon Islands (33%) [12,21]. Most of the impetigo (82%) in this study was very mild, consistent with other studies [12,13]. Impetigo was positively associated with the presence of scabies, although the association was less strong than previously reported [13]. The association between scabies and impetigo in a range of settings warrants further investigation.
However, in our study, more children identified contact with a friend or class member than a household member. Contact between children at school and between friends is likely to be important for disease transmission between children. Contact history questions should be asked in an appropriate way for specific survey settings and participants.
There were several limitations to our study. First, this study only focused on school children and is therefore not generalizable to other age groups. However, as scabies is highly transmissible among household contacts [27] it is likely that there would be a high prevalence amongst the household members of children with scabies. Second, we enrolled 47.5% of students on the school roll, which may have introduced participation bias. The remaining students did not participate because they were away from school or did not provide consent to participate. Those not attending school may have  Fig. 1 Prevalence of scabies and impetigo by age group with 95% confidence intervals been more disadvantaged with an even greater disease burden, possibly leading to an underestimate of the true prevalence. Conversely, it is possible that some families and teachers may have encouraged children with symptoms of scabies or impetigo to participate, which may have led to an overestimate of prevalence. Third, the diagnosis of scabies and impetigo in the study was based on clinical assessment of exposed areas utilizing the IACS Criteria, rather than whole body examination using dermoscopy, microscopy, or skin scrapings. Limited examination may have underestimated the true prevalence, perhaps by up to 10% [28], whereas reliance on clinical signs may have led to some misclassification and overestimate of disease. Children in low-resource settings are disproportionately affected by scabies and impetigo, predisposing them to significant morbidity and mortality. The high prevalence of scabies in this study supports the ongoing need for prevalence studies and identifying communities where the disease is endemic. The significant burden of disease highlights the need for ongoing health promotion activities for scabies and impetigo. The very high prevalence of scabies also supports the urgent implementation of a population-scale control program in the Solomon Islands. Greater appreciation of scabies as a major global contributor to poor health in children may help to improve awareness and access to treatment in settings where scabies is endemic.
Abbreviations ARR: Adjusted risk ratio; CI: Confidence interval; GAS: Group A Streptococcus; IACS: International Alliance for the Control of Scabies; NTDs-: Neglected Tropical Diseases Funding DE, ACS and JMK are supported by fellowships from the National Health and Medical Research Council of Australia. ACS is also supported by the Heart Foundation of Australia. MHO is supported by an Australian Government Research Training Program (RTP) Scholarship. The funders had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.

Availability of data and materials
The datasets used and analyzed during the study are available from the corresponding author on reasonable request.
Ethics approval and consent to participate Ethical approval was granted by the Royal Children's Hospital Melbourne Human Research Ethics Committee (reference number 38099A) and the Solomon Islands Health Research and Ethics Review Board (reference number 05/18). All participants required written informed consent to participate. For children under 16 years of age, written consent from parents or guardians was obtained.

Consent for publication
Written consent was provided for included material.

Competing interests
MM is an editorial board member for BMC Infectious Diseases. There are no other competing interests to declare.