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      Status of soil-transmitted helminth infections in schoolchildren in Laguna Province, the Philippines: Determined by parasitological and molecular diagnostic techniques

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          Abstract

          Background

          Soil-transmitted helminths (STH) are the most common parasitic infections in impoverished communities, particularly among children. Current STH control is through school-based mass drug administration (MDA), which in the Philippines is done twice annually. As expected, MDA has decreased the intensity and prevalence of STH over time. As a result, the common Kato Katz (KK) thick smear method of detecting STH is less effective because it lacks sensitivity in low intensity infections, making it difficult to measure the impact of deworming programs.

          Methodology/Principal findings

          A cross-sectional study was carried out over a four-week period from October 27, 2014 until November 20, 2014 in Laguna province, the Philippines. Stool samples were collected from 263 schoolchildren, to determine the prevalence of STH and compare diagnostic accuracy of multiplex quantitative polymerase chain reaction (qPCR) with the KK. A large discrepancy in the prevalence between the two techniques was noted for the detection of at least one type of STH infection (33.8% by KK vs. 78.3% by qPCR), Ascaris lumbricoides (20.5% by KK vs. 60.8% by qPCR) and Trichuris trichiura (23.6% by KK vs. 38.8% by qPCR). Considering the combined results of both methods, the prevalence of at least one type of helminth infection, A. lumbricoides, and T. trichiura were 83.3%, 67.7%, and 53.6%, respectively. Sensitivity of the qPCR for detecting at least one type of STH infection, A. lumbricoides, and T. trichiura were 94.1%, 89.9%, and 72.3% respectively; whereas KK sensitivity was 40.6%, 30.3%, and 44.0%, respectively. The qPCR method also detected infections with Ancylostoma spp. (4.6%), Necator americanus (2.3%), and Strongyloides stercoralis (0.8%) that were missed by KK.

          Conclusion/Significance

          qPCR may provide new and important diagnostic information to improve assessment of the effectiveness and impact of integrated control strategies particularly in areas where large-scale STH control has led to low prevalence and/or intensity of infection.

          Author summary

          Worldwide, two billion people are estimated to be infected with soil-transmitted helminths (STH). These infections are primarily found in low resource settings and can result in cognitive impairment and growth stunting in children. The current control method is by chemotherapy, usually during large-scale mass drug administrations (MDA); however, this does not prevent re-infection, which can occur rapidly after treatment. The currently used diagnostics lack sensitivity in low intensity infections, resulting in underreporting of STH prevalence. In order to evaluate new control programs aimed at preventing re-infection and decreasing environmental prevalence of STH, more sensitive diagnostics are required. In this study we have shown that qPCR is far more sensitive than the traditionally used Kato-Katz (KK) microscopic technique, suggesting a role for qPCR in assessing control interventions.

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          Most cited references13

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          The global limits and population at risk of soil-transmitted helminth infections in 2010

          Background Understanding the global limits of transmission of soil-transmitted helminth (STH) species is essential for quantifying the population at-risk and the burden of disease. This paper aims to define these limits on the basis of environmental and socioeconomic factors, and additionally seeks to investigate the effects of urbanisation and economic development on STH transmission, and estimate numbers at-risk of infection with Ascaris lumbricoides, Trichuris trichiura and hookworm in 2010. Methods A total of 4,840 geo-referenced estimates of infection prevalence were abstracted from the Global Atlas of Helminth Infection and related to a range of environmental factors to delineate the biological limits of transmission. The relationship between STH transmission and urbanisation and economic development was investigated using high resolution population surfaces and country-level socioeconomic indicators, respectively. Based on the identified limits, the global population at risk of STH transmission in 2010 was estimated. Results High and low land surface temperature and extremely arid environments were found to limit STH transmission, with differential limits identified for each species. There was evidence that the prevalence of A. lumbricoides and of T. trichiura infection was statistically greater in peri-urban areas compared to urban and rural areas, whilst the prevalence of hookworm was highest in rural areas. At national levels, no clear socioeconomic correlates of transmission were identified, with the exception that little or no infection was observed for countries with a per capita gross domestic product greater than US$ 20,000. Globally in 2010, an estimated 5.3 billion people, including 1.0 billion school-aged children, lived in areas stable for transmission of at least one STH species, with 69% of these individuals living in Asia. A further 143 million (31.1 million school-aged children) lived in areas of unstable transmission for at least one STH species. Conclusions These limits provide the most contemporary, plausible representation of the extent of STH risk globally, and provide an essential basis for estimating the global disease burden due to STH infection.
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            The coverage and frequency of mass drug administration required to eliminate persistent transmission of soil-transmitted helminths

            A combination of methods, including mathematical model construction, demographic plus epidemiological data analysis and parameter estimation, are used to examine whether mass drug administration (MDA) alone can eliminate the transmission of soil-transmitted helminths (STHs). Numerical analyses suggest that in all but low transmission settings (as defined by the magnitude of the basic reproductive number, R 0), the treatment of pre-school-aged children (pre-SAC) and school-aged children (SAC) is unlikely to drive transmission to a level where the parasites cannot persist. High levels of coverage (defined as the fraction of an age group effectively treated) are required in pre-SAC, SAC and adults, if MDA is to drive the parasite below the breakpoint under which transmission is eliminated. Long-term solutions to controlling helminth infections lie in concomitantly improving the quality of the water supply, sanitation and hygiene (WASH). MDA, however, is a very cost-effective tool in long-term control given that most drugs are donated free by the pharmaceutical industry for poor regions of the world. WASH interventions, by lowering the basic reproductive number, can facilitate the ability of MDA to interrupt transmission.
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              The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases?

              Parasitic infections are widespread throughout the tropics and sub-tropics, and infection with multiple parasite species is the norm rather than the exception. Despite the ubiquity of polyparasitism, its public health significance has been inadequately studied. Here we review available studies investigating the nutritional and pathological consequences of multiple infections with Plasmodium and helminth infection and, in doing so, encourage a reassessment of the disease burden caused by polyparasitism. The available evidence is conspicuously sparse but is suggestive that multiple human parasite species may have an additive and/or multiplicative impact on nutrition and organ pathology. Existing studies suffer from a number of methodological limitations and adequately designed studies are clearly necessary. Current methods of estimating the potential global morbidity due to parasitic diseases underestimate the health impact of polyparasitism, and possible reasons for this are presented. As international strategies to control multiple parasite species are rolled-out, there is a number of options to investigate the complexity of polyparasitism, and it is hoped that that the parasitological research community will grasp the opportunity to understand better the health of polyparasitism in humans.
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                Author and article information

                Contributors
                Role: Formal analysisRole: InvestigationRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Funding acquisitionRole: Writing – review & editing
                Role: Funding acquisitionRole: Writing – review & editing
                Role: Funding acquisitionRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: 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
                6 November 2017
                November 2017
                : 11
                : 11
                : e0006022
                Affiliations
                [1 ] Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines
                [2 ] Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia
                [3 ] Research School of Population Health, The Australian National University, Canberra, Australia
                [4 ] Discipline of Epidemiology and Biostatistics, School of Public Health, University of Queensland, Brisbane, Australia
                [5 ] Swiss Tropical and Public Health Institute, Basel Switzerland
                [6 ] University of Basel, Basel Switzerland
                [7 ] School of Public Health and Social Work, Queensland University of Technology, Brisbane, Australia
                [8 ] Hunan Institute of Parasitic Diseases, World Health Organization Collaborating Centre for Research and Control on Schistosomiasis in Lake Region, Yueyang, People’s Republic of China
                Vienna, AUSTRIA
                Author notes

                The authors have declared that no competing interests exist.

                ‡ MLSM and CAG share first authorship on this work.

                Article
                PNTD-D-17-00629
                10.1371/journal.pntd.0006022
                5703569
                29108026
                65178054-94bc-440d-8374-08da37dfffab
                © 2017 Mationg 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
                : 1 May 2017
                : 7 October 2017
                Page count
                Figures: 2, Tables: 7, Pages: 16
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;
                Funded by: funder-id http://dx.doi.org/10.13039/501100008391, UBS Optimus Foundation;
                Funded by: funder-id http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;
                Award ID: NHMRC CDF
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;
                Award ID: NHMRC SRF
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;
                Award ID: NHMRC SPRF
                Award Recipient :
                This work is funded by a National Health and Medical Research Council (NHMRC) Australia, project grant (1046901); and the UBS-Optimus Foundation Switzerland. DJG is an Australian NHMRC Career Development Fellow; ACAC is an Australian NHMRC Senior Research Fellow; DPM is an Australian NHMRC Senior Principal Research Fellow. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Ascaris Lumbricoides
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Nematoda
                Ascaris
                Ascaris Lumbricoides
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Medicine and Health Sciences
                Parasitic Diseases
                Social Sciences
                Sociology
                Education
                Schools
                People and Places
                Population Groupings
                Educational Status
                Schoolchildren
                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
                Diagnostic Medicine
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Hookworms
                Necator Americanus
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Nematoda
                Necator
                Necator Americanus
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-11-27
                All relevant data are within the paper and its Supporting Information file.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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