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      Scabies and Impetigo Prevalence and Risk Factors in Fiji: A National Survey

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          Abstract

          Background

          Scabies is recognised as a major public health problem in many countries, and is responsible for significant morbidity due to secondary bacterial infection of the skin causing impetigo, abscesses and cellulitis, that can in turn lead to serious systemic complications such as septicaemia, kidney disease and, potentially, rheumatic heart disease. Despite the apparent burden of disease in many countries, there have been few large-scale surveys of scabies prevalence or risk factors. We undertook a population-based survey in Fiji of scabies and impetigo to evaluate the magnitude of the problem and inform public health strategies.

          Methodology/Principal Findings

          A total of 75 communities, including villages and settlements in both urban and rural areas, were randomly selected from 305 communities across the four administrative divisions, and all residents in each location were invited to participate in skin examination by trained personnel. The study enrolled 10,887 participants. The prevalence of scabies was 23.6%, and when adjusted for age structure and geographic location based on census data, the estimated national prevalence was 18.5%. The prevalence was highest in children aged five to nine years (43.7%), followed by children aged less than five (36.5%), and there was also an indication of prevalence increasing again in older age. The prevalence of scabies was twice as high in iTaukei (indigenous) Fijians compared to Indo-Fijians. The prevalence of impetigo was 19.6%, with a peak in children aged five to nine years (34.2%). Scabies was very strongly associated with impetigo, with an estimated 93% population attributable risk.

          Conclusions

          As far as we are aware, this is the first national survey of scabies and impetigo ever conducted. We found that scabies occurs at high levels across all age groups, ethnicities, and geographical locations. Improved strategies are urgently needed to achieve control of scabies and its complications in endemic communities.

          Author Summary

          Recently added to the World Health Organization list of neglected tropical diseases, scabies is an under-recognised cause of morbidity in many developing countries, due to secondary bacterial infection of the skin that can in turn lead to serious systemic complications such as kidney disease and, potentially, rheumatic heart disease. Despite the apparent burden of disease in many countries, there have been few large-scale surveys of scabies prevalence or risk factors. We undertook a population-based survey in Fiji of scabies and impetigo to evaluate the magnitude of the problem and inform public health strategies. We examined 10,887 people across 75 communities in all four geographical divisions of Fiji, covering both urban and rural areas. The national prevalence of scabies and impetigo was 23.6% and 19.6% respectively, and highest in children aged 5–9 years. We found that scabies was very strongly associated with impetigo. Scabies was twice as high in iTaukei (indigenous) Fijians compared to Indo-Fijians. Our study shows that scabies occurs at high levels across all age groups, ethnicities, and geographical locations. Improved strategies are urgently needed to achieve control of scabies and its complications in endemic communities.

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          Most cited references15

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          The global burden of group A streptococcal diseases.

          The global burden of disease caused by group A streptococcus (GAS) is not known. We review recent population-based data to estimate the burden of GAS diseases and highlight deficiencies in the available data. We estimate that there are at least 517,000 deaths each year due to severe GAS diseases (eg, acute rheumatic fever, rheumatic heart disease, post-streptococcal glomerulonephritis, and invasive infections). The prevalence of severe GAS disease is at least 18.1 million cases, with 1.78 million new cases each year. The greatest burden is due to rheumatic heart disease, with a prevalence of at least 15.6 million cases, with 282,000 new cases and 233,000 deaths each year. The burden of invasive GAS diseases is unexpectedly high, with at least 663,000 new cases and 163,000 deaths each year. In addition, there are more than 111 million prevalent cases of GAS pyoderma, and over 616 million incident cases per year of GAS pharyngitis. Epidemiological data from developing countries for most diseases is poor. On a global scale, GAS is an important cause of morbidity and mortality. These data emphasise the need to reinforce current control strategies, develop new primary prevention strategies, and collect better data from developing countries.
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            Toward the Global Control of Human Scabies: Introducing the International Alliance for the Control of Scabies

            Scabies, the human skin disease caused by infestation by the mite Sarcoptes scabiei var. hominis, causes considerable morbidity and mortality through direct effects and as a result of secondary bacterial infection. Scabies is a truly neglected disease, largely absent from the global health agenda, and its huge burden of disease is largely underappreciated. We contend that coordinated, global efforts to control this ubiquitous pathogenic mite are both important and achievable. Why Is Scabies Important? Scabies affects people of all countries, particularly the most vulnerable sectors of society. Children in developing countries are most susceptible, with an average prevalence of 5–10% [1]. The highest incidence is in tropical climates, with rates of up to 25% overall and up to 50% in some communities in the South Pacific and northern Australia [2], [3]. Poverty and overcrowding are the main risk factors, and outbreaks in institutions and refugee camps are common [4]. Scabies causes intense itch, severely affecting sleep and quality of life [5]. Crusted scabies, a severe infestation with thousands of mites, is associated with extremely high risk of contagion and causes considerable morbidity [6]. The complications and secondary effects of scabies cause a huge public health burden, yet are generally underappreciated (Figure 1) [7], [8]. Infestation is frequently complicated by bacterial skin infection, including impetigo, cellulitis, and abscess due to Streptococcus pyogenes and Staphylococcus aureus (Figure 2). Such bacterial skin infections predispose to serious suppurative and nonsuppurative sequelae. 10.1371/journal.pntd.0002167.g001 Figure 1 Complications of scabies infestation. 10.1371/journal.pntd.0002167.g002 Figure 2 Hand of an adolescent girl in Fiji, demonstrating scabies infestation with typical secondary bacterial infection. Scabies infestation provides an important portal of entry for bacteria, and complement inhibitors from scabies mites promote bacterial growth in vitro [9]. Bacterial skin infection predisposes to sepsis and invasive infections. An estimated 660,000 incident cases of invasive S. pyogenes occur globally each year, leading to more than 160,000 deaths [10], and the numbers are probably at least as great for S. aureus. Skin infection with S. pyogenes can also lead to the nonsuppurative complications of acute post-streptococcal glomerulonephritis (APSGN) and possibly acute rheumatic fever. Skin infection is responsible for approximately 50% of APSGN in tropical settings [1], estimated at more than 470,000 cases per year [10]. Outbreaks of APSGN coincide with those of scabies [11], and asymptomatic renal disease is also common [12]. These insults to the kidney in childhood contribute to the development of chronic kidney disease and subsequent renal failure in adulthood [13]. Community control of scabies, even without interventions targeting bacterial skin infection, has been shown to reduce rates of both streptococcal skin infection and haematuria [12]. The relationship between scabies, streptococcal skin infection, and acute rheumatic fever requires further examination, but offers one potential explanation for the high rates of rheumatic heart disease in countries with high rates of scabies and impetigo, but low rates of streptococcal pharyngitis [14]. Scabies imposes a considerable economic burden on individuals, families, communities, and health systems. Families in endemic areas spend a substantial portion of income on treatments, restricting available funds for food and essential commodities [15], [16]. Direct costs relate to treatments, missed employment, frequent healthcare consultations, and management of hospitalised cases including institutional outbreaks. Further information is needed to quantify the indirect costs, including complications in later life. Current Strategies to Treat and Control Scabies Current management of scabies is centred on identification and treatment of cases and household contacts, but there is a paucity of data to support this as an effective strategy for reducing scabies prevalence. Diagnosis can be difficult and is reliant on clinical identification in most tropical areas [4]. Topical treatments are effective, but the most effective of these, permethrin [17], is expensive [18] and unavailable in many high-prevalence areas. Alternative treatments may be less effective, poorly tolerated, or have more substantial adverse effects. Topical regimens are inconvenient, and low compliance among household contacts may reduce the effectiveness of contact treatment, leading to reinfestation [19]. Steps toward Global Control of Scabies We contend that global control of scabies is achievable, despite a number of impediments. Initial priorities include: i) raising awareness of scabies and engaging financial supporters through advocacy; ii) enhanced clinical and epidemiologic study to better understand the burden of disease; and iii) development and implementation of effective control strategies. An enhanced and coordinated research program that involves active collaboration among a diverse group of stakeholders is crucial to underpin all of these areas. The first challenge is to raise the profile of this ubiquitous but largely ignored disease. There are a number of hurdles to overcome to achieve this goal; two are mentioned here. First, endemic scabies is primarily a disease of tropical developing countries, where resources are scarce and where there are numerous competing health priorities, often with apparent higher direct morbidity and mortality. Second, the impact is spread across a broad range of clinical disciplines including dermatology, infectious diseases, and paediatrics, with long-term sequelae spread between nephrology and cardiology. The World Health Organization (WHO) recognises the need for specific programs to target neglected tropical diseases (NTDs), which affect more than 1 billion people and frequently cluster and overlap in individuals and regions [20]. The Special Programme for Research and Training in Tropical Diseases (TDR) has released a global report for research on global diseases of poverty, including an agenda for change [21]. Scabies is not included in this report. We strongly contend that scabies be added to the WHO list of global NTDs [22]. Acknowledgment of scabies as an important communicable disease of poverty will promote research interest, engage donors, and encourage the integrated framework for NTD control to encompass scabies control. It is essential to establish an accurate estimate of the global burden of scabies, from individual health (including renal and cardiac morbidity) to the impact on the community and region. Interpretation of the few epidemiological studies published to date is confounded by differences in methodology and the lack of harmonised diagnostic criteria. Priorities include development of validated, practical criteria for diagnosis [23], [24]; the establishment of accurate national and international reporting systems; quantification of the impact on health and economic activity; and further research into proposed associations with serious health conditions such as invasive bacterial infections, APSGN, and rheumatic fever. Control strategies will require innovation, leadership, collaboration, and a considerable increase in available resources. Successful long-term control must involve addressing the underlying social determinants of poverty and overcrowding, and this should be reflected in policy and advocacy [21]. There is clear overlap with other NTDs across a range of domains, including mapping, surveillance, and effective systemic treatments, and therefore the ideal control strategy for scabies would be integrated within the global and regional strategy for other NTDs. New approaches to control, including mass drug administration, are cause for some optimism. Mass administration studies in Panama and northern Australia have shown that topical permethrin substantially reduced scabies and impetigo prevalence [25]–[27]. Mass treatment with oral ivermectin in the Solomon Islands reduced scabies prevalence from 25% to 1%, with concomitant reductions in impetigo and haematuria [12]. Oral ivermectin is an effective treatment for scabies, commonly used for crusted scabies and institutional outbreaks. Ivermectin has a long history of use, with more than 1 billion doses distributed by control programs for onchocerciasis and filiariasis [28], [29], and the possibility of incorporating scabies treatment within control strategies for other NTDs is attractive. However, important issues regarding ivermectin must be addressed, including potential for resistance [30], [31], cost-effectiveness, and use in potentially pregnant women and small children. Further, despite its well-documented efficacy, ivermectin is not licensed for, or available for, treatment of scabies in many countries. Novel treatments such as other macrocylic lactones (e.g., oral moxidectin) and topical herbal compounds warrant further investigation [4]. Ensuring a supply of medications to treat scabies and associated skin diseases in endemic regions will be critical. Research is needed to inform each aspect of control, including biological research into transmission and pathogenesis, clinical research into diagnosis and treatment, epidemiologic research into downstream effects, and public health research to investigate sustainable and effective control programs. An audit and publication of current global research, both biological and clinical, is important to promote collaboration and integration of knowledge from diverse fields. The recently formed Sarcoptes-World Molecular Network, consisting of parasitologists from all continents, aims to be a facilitator of molecular and genetic research on Sarcoptes species in humans and animals [32]. International Alliance for the Control of Scabies The International Alliance for the Control of Scabies (IACS) is a recently formed group from across the globe to advance the agenda of scabies control. The alliance is committed to the control of human scabies infestation, and to promoting the health and well-being of all those living in affected communities. Initial membership includes a diverse range of professionals including clinicians from high-prevalence areas, public health physicians, policy makers, and researchers studying the biology of the parasite, and continues to grow with identification and recruitment of further collaborators. Our first international meeting was held in November 2012. Representatives from five continents exchanged ideas on the priority areas of advocacy, epidemiology, control strategies, and biological research, and have developed working groups and an action plan to progress these themes. There are many obstacles on the road toward control of human scabies, but the effects on children, families, and communities worldwide, particularly the underappreciated downstream effects, are a strong impetus for us to embark on the campaign. The willingness of the global community to collaborate and work together toward this goal gives us reason to be optimistic, and we hope that IACS can provide a focus for future efforts for this most neglected of diseases.
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              Control of scabies, skin sores and haematuria in children in the Solomon Islands: another role for ivermectin.

              To assess the effects of a 3-year programme aimed at controlling scabies on five small lagoon islands in the Solomon Islands by monitoring scabies, skin sores, streptococcal skin contamination, serology and haematuria in the island children. Control was achieved by treating almost all residents of each island once or twice within 2 weeks with ivermectin (160-250 microg/kg), except for children who weighed less than 15 kg and pregnant women, for whom 5% permethrin cream was used. Reintroduction of scabies was controlled by treating returning residents and visitors, whether or not they had evident scabies. Prevalence of scabies dropped from 25% to less than 1% (P < 0.001); prevalence of sores from 40% to 21% (P < 0.001); streptococcal contamination of the fingers in those with and without sores decreased significantly (P = 0.02 and 0.047, respectively) and anti-DNase B levels decreased (P = 0.002). Both the proportion of children with haematuria and its mean level fell (P = 0.002 and P < 0.001, respectively). No adverse effects of the treatments were seen. The results show that ivermectin is an effective and practical agent in the control of scabies and that control reduces the occurrence of streptococcal skin disease and possible signs of renal damage in children. Integrating community-based control of scabies and streptococcal skin disease with planned programmes for controlling filariasis and intestinal nematodes could be both practical and produce great health benefits.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                4 March 2015
                March 2015
                : 9
                : 3
                : e0003452
                Affiliations
                [1 ]Kirby Institute, University of New South Wales, Sydney, Australia
                [2 ]Ministry for Social Welfare, Suva, Fiji
                [3 ]Centre for International Child Health, University of Melbourne, Australia
                [4 ]Ministry of Health, Suva, Fiji
                [5 ]Mugda 500 Bed General Hospital, Dhaka, Bangladesh
                [6 ]Department of Dermatology, St Vincent’s Hospital, Sydney, Australia
                Queensland Institute for Medical Research, AUSTRALIA
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LR MJW JK MH MK. Performed the experiments: LR. Analyzed the data: LR HW. Contributed reagents/materials/analysis tools: MK. Wrote the paper: LR ACS MJW JMK. Designed the software used in analysis: LR AS.

                Article
                PNTD-D-14-01489
                10.1371/journal.pntd.0003452
                4349858
                25738499
                193cb936-0544-4740-9f77-8e9039f8f5f1
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 28 August 2014
                : 1 December 2014
                Page count
                Figures: 1, Tables: 4, Pages: 10
                Funding
                Funding for this project was through the financial contributions of Ian and Barbara Jackson, David Gray, Peter Nash and Margot Whitfeld. Funding from these individuals was used for salaries of research staff and for purchase of consumables required to conduct the field visits. They funded this research as private individuals. Margot Whitfeld is an investigator and author on the study and therefore she had a role in study design, data collection and analysis, decision to publish, and preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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