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      Albendazole and ivermectin for the control of soil-transmitted helminths in an area with high prevalence of Strongyloides stercoralis and hookworm in northwestern Argentina: A community-based pragmatic study

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          Abstract

          Background

          Recommendations for soil-transmitted helminth (STH) control give a key role to deworming of school and pre-school age children with albendazole or mebendazole; which might be insufficient to achieve adequate control, particularly against Strongyloides stercoralis. The impact of preventive chemotherapy (PC) against STH morbidity is still incompletely understood. The aim of this study was to assess the effectiveness of a community-based program with albendazole and ivermectin in a high transmission setting for S. stercoralis and hookworm.

          Methodology

          Community-based pragmatic trial conducted in Tartagal, Argentina; from 2012 to 2015. Six communities (5070 people) were enrolled for community-based PC with albendazole and ivermectin. Two communities (2721 people) were re-treated for second and third rounds. STH prevalence, anemia and malnutrition were explored through consecutive surveys. Anthropometric assessment of children, stool analysis, complete blood count and NIE-ELISA serology for S. stercoralis were performed.

          Principal findings

          STH infection was associated with anemia and stunting in the baseline survey that included all communities and showed a STH prevalence of 47.6% (almost exclusively hookworm and S. stercoralis). Among communities with multiple interventions, STH prevalence decreased from 62% to 23% (p<0.001) after the first PC; anemia also diminished from 52% to 12% (p<0.001). After two interventions S. stercoralis seroprevalence declined, from 51% to 14% (p<0.001) and stunting prevalence decreased, from 19% to 12% (p = 0.009).

          Conclusions

          Hookworm’ infections are associated with anemia in the general population and nutritional impairment in children. S. stercoralis is also associated with anemia. Community-based deworming with albendazole and ivermectin is effective for the reduction of STH prevalence and morbidity in communities with high prevalence of hookworm and S. stercoralis.

          Author summary

          Soil-transmitted helminth (STH) infections are a relevant public health problem in resource restricted settings due to their potential to perpetuate poverty, since chronic infections are associated with learning and grow impairment in children and reduced productivity in adults. The current strategy for STH control gives a key role to preventive chemotherapy of risk groups (preschool and school age children and women of childbearing age) with anthelmintic drugs. The drugs recommended for regular deworming are albendazole or mebendazole. This strategy does not target Strongyloides stercoralis, an STH resistant to the recommended drugs in single doses. The efficacy of ivermectin, alone or in combination, for the treatment of Strongyloides stercoralis infection has been reported in controlled trials. We conducted a pragmatic study aiming to assess the effectiveness of community based preventive chemotherapy with albendazole plus ivermectin for the control of STH prevalence and morbidity, in endemic communities of Northwestern Argentina. We found high baseline prevalence of hookworm and Strongyloides stercoralis and significant nutritional and hematological morbidity associated with these infections. After three rounds of preventive chemotherapy with albendazole and ivermectin we observed a significant decline in the prevalence of infection and in the prevalence and severity of morbidity.

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          Most cited references 46

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          Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm.

          The three main soil-transmitted helminth infections, ascariasis, trichuriasis, and hookworm, are common clinical disorders in man. The gastrointestinal tract of a child living in poverty in a less developed country is likely to be parasitised with at least one, and in many cases all three soil-transmitted helminths, with resultant impairments in physical, intellectual, and cognitive development. The benzimidazole anthelmintics, mebendazole and albendazole, are commonly used to remove these infections. The use of these drugs is not limited to treatment of symptomatic soil-transmitted helminth infections, but also for large-scale prevention of morbidity in children living in endemic areas. As a result of data showing improvements in child health and education after deworming, and the burden of disease attributed to soil-transmitted helminths, the worldwide community is awakening to the importance of these infections. Concerns about the sustainability of periodic deworming with benzimidazole anthelmintics and the emergence of resistance have prompted efforts to develop and test new control tools.
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            Global epidemiology, ecology and control of soil-transmitted helminth infections.

            Soil-transmitted helminth (STH) infections are among the most prevalent of chronic human infections worldwide. Based on the demonstrable impact on child development, there is a global commitment to finance and implement control strategies with a focus on school-based chemotherapy programmes. The major obstacle to the implementation of cost-effective control is the lack of accurate descriptions of the geographical distribution of infection. In recent years, considerable progress has been made in the use of geographical information systems (GIS) and remote sensing (RS) to better understand helminth ecology and epidemiology, and to develop low-cost ways to identify target populations for treatment. This review explores how this information has been used practically to guide large-scale control programmes. The use of satellite-derived environmental data has yielded new insights into the ecology of infection at a geographical scale that has proven impossible to address using more traditional approaches, and has in turn allowed spatial distributions of infection prevalence to be predicted robustly by statistical approaches. GIS/RS have increasingly been used in the context of large-scale helminth control programmes, including not only STH infections but also those focusing on schistosomiasis, filariasis and onchocerciasis. The experience indicates that GIS/RS provides a cost-effective approach to designing and monitoring programmes at realistic scales. Importantly, the use of this approach has begun to transition from being a specialist approach of international vertical programmes to becoming a routine tool in developing public sector control programmes. GIS/RS is used here to describe the global distribution of STH infections and to estimate the number of infections in school-age children in sub-Saharan Africa (89.9 million) and the annual cost of providing a single anthelmintic treatment using a school-based approach (US$5.0-7.6 million). These are the first estimates at a continental scale to explicitly include the fine spatial distribution of infection prevalence and population, and suggest that traditional methods have overestimated the situation. The results suggest that continent-wide control of parasites is, from a financial perspective, an attainable goal.
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              Strongyloidiasis--the most neglected of the neglected tropical diseases?

              Soil-transmitted helminths of the genus Strongyloides (S. fuelleborni and the more prevalent S. stercoralis) are currently believed to infect an estimated 30-100 million people worldwide. The health consequences of S. stercoralis infections range from asymptomatic light infections to chronic symptomatic strongyloidiasis. Uncontrolled multiplication of the parasite (hyperinfection) and potentially life-threatening dissemination of larvae to all internal organs is found among individuals with compromised immune system functions. This paper provides an overview of the current state of the art in relation to diagnostic methods for detecting the infection, the morbidity caused by the infection and the recommended treatment. It further discusses some of the reasons why this infection is so neglected and the consequence of this for the estimated global prevalence. The paper finally points to the gaps in our knowledge and future research needs related to this infection. As Strongyloides infections have the potential to develop into severe disease in certain population subgroups, untreated infections could cause serious problems in the community. Therefore, we need to carefully investigate this parasite in order to develop and implement effective control programmes.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ValidationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: 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
                9 October 2017
                October 2017
                : 11
                : 10
                Affiliations
                [1 ] Instituto de Investigaciones en Enfermedades Tropicales, Universidad Nacional de Salta-Sede Regional Orán, San Ramón de la Nueva Orán, Salta, Argentina
                [2 ] Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
                [3 ] Facultad de Ciencias Naturales, Cátedra de Química Biológica, Universidad Nacional de Salta, Salta, Argentina
                [4 ] Gerencia Sanitaria, Hospital Juan Domingo Perón, Tartagal, Salta, Argentina
                [5 ] Secretaria de Nutrición y Alimentación Saludable, Ministerio de Salud Pública de la Provincia de Salta, Salta, Argentina
                [6 ] Departamento de Programas y Proyectos, Fundación Mundo Sano, Buenos Aires, Argentina
                [7 ] Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America
                University of Queensland, AUSTRALIA
                Author notes

                The authors have declared that no competing interests exist.

                Article
                PNTD-D-17-00976
                10.1371/journal.pntd.0006003
                5648268
                28991899

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                Counts
                Figures: 6, Tables: 4, Pages: 20
                Product
                Funding
                Fundación Mundo Sano ( https://www.mundosano.org) provided funding for this study through an unrestricted grant (UNSa.IIET.2012). Two of the co-authors (MA and SG) are members of Fundación Mundo Sano, their participation in the study was limited to study design and revision and approval of the final version of the article before submission. Fundación Mundo Sano had no role in the patients recruitment; data collection, analysis and interpretation; writing, and decision to submit for publication.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Nematoda
                Strongyloides
                Strongyloides Stercoralis
                Medicine and Health Sciences
                Hematology
                Anemia
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Hookworms
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Soil-Transmitted Helminthiases
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Soil-Transmitted Helminthiases
                Medicine and Health Sciences
                Health Care
                Health Statistics
                Morbidity
                Medicine and Health Sciences
                Public and Occupational Health
                People and Places
                Population Groupings
                Age Groups
                Children
                People and Places
                Population Groupings
                Families
                Children
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-10-19
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology

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