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      High burden and seasonal variation of paediatric scabies and pyoderma prevalence in The Gambia: A cross-sectional study

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          Abstract

          Background

          Scabies is a WHO neglected tropical disease common in children in low- and middle-income countries. Excoriation of scabies lesions can lead to secondary pyoderma infection, most commonly by Staphyloccocus aureus and Streptococcus pyogenes (group A streptococcus, GAS), with the latter linked to acute post-streptococcal glomerulonephritis (APSGN) and potentially rheumatic heart disease (RHD). There is a paucity of data on the prevalence of these skin infections and their bacterial aetiology from Africa.

          Methodology/Principal findings

          A cross-sectional study, conducted over a four-month period that included the dry and rainy season, was conducted to determine the prevalence of common skin infections in Sukuta, a peri-urban settlement in western Gambia, in children <5 years. Swabs from pyoderma lesions were cultured for S. aureus and GAS. Of 1441 children examined, 15.9% had scabies (95% CI 12.2–20.4), 17.4% had pyoderma (95% CI 10.4–27.7) and 9.7% had fungal infections (95% CI 6.6–14.0). Scabies was significantly associated with pyoderma (aOR 2.74, 95% CI 1.61–4.67). Of 250 pyoderma swabs, 80.8% were culture-positive for S. aureus, and 50.8% for GAS. Participants examined after the first rains were significantly more likely to have pyoderma than those examined before (aRR 2.42, 95% CI 1.38–4.23), whereas no difference in scabies prevalence was seen (aRR 1.08, 95% CI 0.70–1.67). Swab positivity was not affected by the season.

          Conclusions/Significance

          High prevalence of scabies and pyoderma were observed. Pyoderma increased significantly during the rainy season. Given the high prevalence of GAS pyoderma among children, further research on the association with RHD in West Africa is warranted.

          Author summary

          Scabies is a WHO neglected tropical disease which is common in low- and middle-income countries with tropical climates, which can lead to serious compilations via secondary bacterial infection of skin lesions. Group A streptococcal skin infection is known to cause kidney disease, but may also contribute to rheumatic heart disease. Despite this, little is known about the prevalence of common paediatric skin infections in sub-Saharan Africa, or which bacteria most commonly cause skin infections. We conducted a cross-sectional study of skin infections in The Gambia into the prevalence of scabies, pyoderma and fungal infections in children <5 years. We examined 1441 children and found a scabies, pyoderma and fungal infection prevalence of 15.9%, 17.4% and 9.7% respectively, with significantly increased presence of bacterial skin infections in the rainy season. Over half of bacterial skin infections were found to be positive for group A streptococcus. Our study shows that scabies and pyoderma occur commonly in young children in The Gambia, representing a significant exposure to group A streptococcus at a young age, and that there is a strong seasonal effect on pyoderma, which may have implications for treatment strategies.

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          Most cited references43

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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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            Global, Regional, and National Burden of Rheumatic Heart Disease, 1990-2015.

            Rheumatic heart disease remains an important preventable cause of cardiovascular death and disability, particularly in low-income and middle-income countries. We estimated global, regional, and national trends in the prevalence of and mortality due to rheumatic heart disease as part of the 2015 Global Burden of Disease study.
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              Disease manifestations and pathogenic mechanisms of group a Streptococcus.

              Streptococcus pyogenes, also known as group A Streptococcus (GAS), causes mild human infections such as pharyngitis and impetigo and serious infections such as necrotizing fasciitis and streptococcal toxic shock syndrome. Furthermore, repeated GAS infections may trigger autoimmune diseases, including acute poststreptococcal glomerulonephritis, acute rheumatic fever, and rheumatic heart disease. Combined, these diseases account for over half a million deaths per year globally. Genomic and molecular analyses have now characterized a large number of GAS virulence determinants, many of which exhibit overlap and redundancy in the processes of adhesion and colonization, innate immune resistance, and the capacity to facilitate tissue barrier degradation and spread within the human host. This improved understanding of the contribution of individual virulence determinants to the disease process has led to the formulation of models of GAS disease progression, which may lead to better treatment and intervention strategies. While GAS remains sensitive to all penicillins and cephalosporins, rising resistance to other antibiotics used in disease treatment is an increasing worldwide concern. Several GAS vaccine formulations that elicit protective immunity in animal models have shown promise in nonhuman primate and early-stage human trials. The development of a safe and efficacious commercial human vaccine for the prophylaxis of GAS disease remains a high priority.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Supervision
                Role: InvestigationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Supervision
                Role: InvestigationRole: ResourcesRole: Supervision
                Role: InvestigationRole: ResourcesRole: Supervision
                Role: MethodologyRole: Writing – review & editing
                Role: Data curationRole: ResourcesRole: Writing – review & editing
                Role: Funding acquisitionRole: MethodologyRole: Writing – review & editing
                Role: Funding acquisitionRole: Resources
                Role: Funding acquisitionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                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
                14 October 2019
                October 2019
                : 13
                : 10
                : e0007801
                Affiliations
                [1 ] Medical Research Council Unit The Gambia at The London School of Hygiene & Tropical Medicine, Banjul, The Gambia
                [2 ] Department of Clinical Research, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom
                [3 ] Department of Molecular Biology & Biotechnology, The Florey Institute, University of Sheffield, Sheffield, United Kingdom
                [4 ] Department of Infection, Immunity and Cardiovascular Diseases, The Florey Institute, University of Sheffield, Sheffield, United Kingdom
                Hitit University, Faculty of Medicine, TURKEY
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-1125-4260
                http://orcid.org/0000-0002-4711-3307
                http://orcid.org/0000-0002-5237-8852
                Article
                PNTD-D-19-00695
                10.1371/journal.pntd.0007801
                6812840
                31609963
                d8dec76f-2c3e-4b5b-b87c-940559caa7b9
                © 2019 Armitage et al

                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
                : 3 May 2019
                : 20 September 2019
                Page count
                Figures: 2, Tables: 3, Pages: 16
                Funding
                This work was supported by a HEFCE/ODA grant from The University of Sheffield (155123). TIdS in funded by a Wellcome Trust Intermediate Clinical Fellowship award [110058/ Z/15/Z]. CET is a Royal Society & Wellcome Trust Sir Henry Dale Fellow [208765/Z/17/Z ]. MM is supported by an NIHR Clinical Lectureship. Research at the MRC Unit The Gambia at LSHTM is jointly funded by the UK Medical Research Council (MRC) and the UK Department for International Development (DFID) under the MRC/DFID Concordat agreement and is also part of the EDCTP2 programme supported by the European Union. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Dermatology
                Pyoderma
                Medicine and Health Sciences
                Parasitic Diseases
                Ectoparasitic Infections
                Scabies
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Scabies
                Medicine and Health Sciences
                Infectious Diseases
                Sexually Transmitted Diseases
                Scabies
                Medicine and Health Sciences
                Dermatology
                Skin Infections
                Medicine and Health Sciences
                Infectious Diseases
                Skin Infections
                Medicine and Health Sciences
                Infectious Diseases
                Fungal Diseases
                Earth Sciences
                Seasons
                Medicine and health sciences
                Infectious diseases
                Bacterial diseases
                Group A streptococcal infection
                Biology and Life Sciences
                Organisms
                Bacteria
                Staphylococcus
                Staphylococcus Aureus
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Staphylococcus
                Staphylococcus Aureus
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Staphylococcus
                Staphylococcus Aureus
                Medicine and Health Sciences
                Epidemiology
                Medical Risk Factors
                Custom metadata
                vor-update-to-uncorrected-proof
                2019-10-24
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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