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      Results of the first mapping of soil-transmitted helminths in Benin: Evidence of countrywide hookworm predominance

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          Abstract

          Background

          National mapping of soil-transmitted helminth infections (STH) was conducted for the first time in all of the 77 districts of Benin (West Africa) from 2013 to 2015. This mapping aimed to provide basic epidemiological data essential for the implementation of the national strategy against the neglected tropical diseases (NTDs) in the context of achieving the WHO target of controlling these infections by 2020.

          Methods

          In each district, 5 schools were purposively selected in 5 villages and 50 school-children (25 girls and 25 boys) from ages 8 to 14 years were randomly enrolled in each school. In total, 19,250 stool samples of school children (9,625 girls and 9,625 boys) from 385 schools were examined by Kato-Katz technique.

          Results

          The three major species of STH (hookworm, Ascaris lumbricoides and Trichuris trichiura) were observed with intra- and inter-specific variations in the prevalence and the intensity of these parasites. Hookworm infection was present in all of the surveyed districts with an average prevalence of 17.14% (95% CI 16.6%-17.6%). Among the infected schoolchildren, at national level, 90.82%, 6.73% and 2.45% of infections were of light, moderate and heavy parasite intensities respectively. A. lumbricoides infection, with a national average prevalence of 5.35% (95% CI 5.00%-5.60%),was the second most prevalent STH, and 84.37%, 14.27% and 1.36% of the infections were of light, moderate and heavy parasite intensities, respectively. T. trichiura had a national average prevalence of 1.15% (95% CI 0.90%-1.20%) and 80.45%, 13.18% and 6.36% infections were of light, moderate and heavy parasite intensities, respectively. The national cumulative prevalence of the three STH infections was 22.74% (95% CI 22.15%-23.33%), with58.44% (45/77) of the districts requiring mass treatment according to WHO recommendations. In all of the surveyed districts, multiple infections by STH species were common, and boys seemed more at risk of hookworm and Ascaris infections.

          Conclusions

          This first national mapping provided an overview of the epidemiological pattern of STH infections and was essential for the implementation of a control strategy with an effective preventive chemotherapy treatment (PCT). Results show that while preventive chemotherapy is not indicated for children in 32/77 districts, 43 require annual deworming and two require twice yearly deworming. If no environmental change occurs, and no mass treatment is delivered, prevalence is likely to remain stable for many years owing to poor hygiene and sanitation.

          Author summary

          Benin, like other low or moderate-income countries in the African continent, is endemic for several neglected tropical diseases, including soil-transmitted helminthiases. The National Program for Neglected Tropical Diseases of the Ministry of Health has conducted the national STH mapping using the Kato-Katz method to assess the baseline epidemiological status in all 77 districts of Benin, in order to guide implementation of a preventive chemotherapy program using albendazole. The results of the survey showed that infection with at least one of the three targeted species (hookworm, roundworm or whipworm) affected 20% or more of school aged children in 45 out of 77 districts, and which therefore require PCT. Hookworm infection was the most prevalent followed by ascariasis and trichuriasis. Boys were significantly more likely than girls to be infected with hookworm or ascariasis.

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          Most cited references18

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          Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a 'gold standard'.

          The accuracy of the Kato-Katz technique in identifying individuals with soil-transmitted helminth (STH) infections is limited by day-to-day variation in helminth egg excretion, confusion with other parasites and the laboratory technicians' experience. We aimed to estimate the sensitivity and specificity of the Kato-Katz technique to detect infection with Ascaris lumbricoides, hookworm and Trichuris trichiura using a Bayesian approach in the absence of a 'gold standard'. Data were obtained from a longitudinal study conducted between January 2004 and December 2005 in Samar Province, the Philippines. Each participant provided between one and three stool samples over consecutive days. Stool samples were examined using the Kato-Katz technique and reported as positive or negative for STHs. In the presence of measurement error, the true status of each individual is considered as latent data. Using a Bayesian method, we calculated marginal posterior densities of sensitivity and specificity parameters from the product of the likelihood function of observed and latent data. A uniform prior distribution was used (beta distribution: alpha=1, beta=1). A total of 5624 individuals provided at least one stool sample. One, two and three stool samples were provided by 1582, 1893 and 2149 individuals, respectively. All STHs showed variation in test results from day to day. Sensitivity estimates of the Kato-Katz technique for one stool sample were 96.9% (95% Bayesian Credible Interval [BCI]: 96.1%, 97.6%), 65.2% (60.0%, 69.8%) and 91.4% (90.5%, 92.3%), for A. lumbricoides, hookworm and T. trichiura, respectively. Specificity estimates for one stool sample were 96.1% (95.5%, 96.7%), 93.8% (92.4%, 95.4%) and 94.4% (93.2%, 95.5%), for A. lumbricoides, hookworm and T. trichiura, respectively. Our results show that the Kato-Katz technique can perform with reasonable accuracy with one day's stool collection for A. lumbricoides and T. trichiura. Low sensitivity of the Kato-Katz for detection of hookworm infection may be related to rapid degeneration of delicate hookworm eggs with time. (c) 2009 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
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            Mass deworming to improve developmental health and wellbeing of children in low-income and middle-income countries: a systematic review and network meta-analysis.

            Soil-transmitted helminthiasis and schistosomiasis, considered among the neglected tropical diseases by WHO, affect more than a third of the world's population, with varying intensity of infection. We aimed to evaluate the effects of mass deworming for soil-transmitted helminths (with or without deworming for schistosomiasis or co-interventions) on growth, educational achievement, cognition, school attendance, quality of life, and adverse effects in children in endemic helminth areas.
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              FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans.

              Hookworms infect more than 10% of the world's population, but current diagnostic tools have drawbacks. Our objective was to compare the diagnostic performance of three methods (Kato-Katz, ether concentration and FLOTAC techniques) for hookworm diagnosis. Stool samples were obtained from 102 schoolchildren in Côte d'Ivoire. First, a duplicate 41.7mg Kato-Katz thick smear was prepared. Next, a small portion of stool (mean weight 1.8g) was preserved in sodium acetate-acetic acid-formalin and forwarded to a European laboratory. These samples were split in three parts, one processed by an ether concentration technique and two by the FLOTAC technique. All samples were examined by experienced technicians for hookworm eggs using light microscopy. The observed hookworm prevalences as assessed by the FLOTAC, Kato-Katz and ether concentration techniques were 65.7%, 51.0% and 28.4%, respectively. Considering the combined results as the diagnostic 'gold' standard, the FLOTAC technique had a sensitivity of 88.2% compared with 68.4% for the Kato-Katz and 38.2% for the ether concentration techniques. The Kato-Katz method resulted in a significantly higher mean number of eggs per gram of stool (155.8 EPG) compared with the FLOTAC (37.7 EPG) and ether concentration (5.7 EPG) methods. The FLOTAC method shows promise as an important new tool for individual hookworm diagnosis and for rigorous monitoring of helminth control programmes. [Clinical Trial No. ISRCTN21782274].
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – original draft
                Role: Formal analysisRole: MethodologyRole: SoftwareRole: ValidationRole: Visualization
                Role: Funding acquisitionRole: MethodologyRole: Project administrationRole: Validation
                Role: MethodologyRole: SoftwareRole: SupervisionRole: Visualization
                Role: Data curationRole: InvestigationRole: SoftwareRole: Supervision
                Role: Formal analysisRole: MethodologyRole: SoftwareRole: Supervision
                Role: ConceptualizationRole: Funding acquisitionRole: ResourcesRole: SupervisionRole: Visualization
                Role: ValidationRole: Visualization
                Role: ValidationRole: Visualization
                Role: Funding acquisitionRole: Project administrationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: VisualizationRole: 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
                1 March 2018
                March 2018
                : 12
                : 3
                : e0006241
                Affiliations
                [1 ] National Control Program of Communicable Diseases, Ministry of Health of Benin, Cotonou, Benin
                [2 ] Department of Zoology, Faculty of Sciences and Techniques, University of Abomey-Calavi, Cotonou, Benin
                [3 ] Research Triangle Institute, Washington, District of Columbia, United States of America, Research Triangle Park, NC, United States of America
                [4 ] Department of Parasitology and Mycology, Faculty of Health Sciences, University of Abomey-Calavi, Cotonou, Benin
                Yale School of Public Health, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                [¤]

                Current address: National Institute of Allergy and Infectious Diseases, National Institute of Health, Maryland, United States of America.

                Author information
                http://orcid.org/0000-0002-3640-0175
                Article
                PNTD-D-17-01028
                10.1371/journal.pntd.0006241
                5849360
                29494579
                c49cbf2d-24b0-440a-98e3-4f37b9a5384f
                © 2018 Ibikounlé 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
                : 27 June 2017
                : 17 January 2018
                Page count
                Figures: 0, Tables: 4, Pages: 17
                Funding
                Funded by: RTI/ENVISION project/United States Agency for International Development (US)
                Award ID: No 0213210-000-012-003
                This study was made possible with funding from the United States Agency for International Development (USAID). USAID support for NTD control in Benin led by RTI International under Cooperative Agreement No 0213210-000-012-003 through the ENVISION project. The contents of this manuscript are the responsibility of the authors and do not necessarily reflect the views of USAID or RTI or the United States Government. The funder 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
                Parasitic Diseases
                Helminth Infections
                Medicine and Health Sciences
                Parasitic Diseases
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Hookworms
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Soil-Transmitted Helminthiases
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Soil-Transmitted Helminthiases
                People and Places
                Geographical Locations
                Africa
                Benin
                Social Sciences
                Sociology
                Education
                Schools
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Nematoda
                Ascaris
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Ascaris Lumbricoides
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Nematoda
                Ascaris
                Ascaris Lumbricoides
                Custom metadata
                vor-update-to-uncorrected-proof
                2018-03-13
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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