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      Heterogeneity in transmission parameters of hookworm infection within the baseline data from the TUMIKIA study in Kenya

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          Abstract

          Background

          As many countries with endemic soil-transmitted helminth (STH) burdens achieve high coverage levels of mass drug administration (MDA) to treat school-aged and pre-school-aged children, understanding the detailed effects of MDA on the epidemiology of STH infections is desirable in formulating future policies for morbidity and/or transmission control. Prevalence and mean intensity of infection are characterized by heterogeneity across a region, leading to uncertainty in the impact of MDA strategies. In this paper, we analyze this heterogeneity in terms of factors that govern the transmission dynamics of the parasite in the host population.

          Results

          Using data from the TUMIKIA study in Kenya (cluster STH prevalence range at baseline: 0–63%), we estimated these parameters and their variability across 120 population clusters in the study region, using a simple parasite transmission model and Gibbs-sampling Monte Carlo Markov chain techniques. We observed great heterogeneity in R 0 values, with estimates ranging from 1.23 to 3.27, while k-values (which vary inversely with the degree of parasite aggregation within the human host population) range from 0.007 to 0.29 in a positive association with increasing prevalence. The main finding of this study is the increasing trend for greater parasite aggregation as prevalence declines to low levels, reflected in the low values of the negative binomial parameter k in clusters with low hookworm prevalence. Localized climatic and socioeconomic factors are investigated as potential drivers of these observed epidemiological patterns.

          Conclusions

          Our results show that lower prevalence is associated with higher degrees of aggregation and hence prevalence alone is not a good indicator of transmission intensity. As a consequence, approaches to MDA and monitoring and evaluation of community infection status may need to be adapted as transmission elimination is aimed for by targeted treatment approaches.

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          Most cited references35

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          WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas

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            Global numbers of infection and disease burden of soil transmitted helminth infections in 2010

            Background Quantifying the burden of parasitic diseases in relation to other diseases and injuries requires reliable estimates of prevalence for each disease and an analytic framework within which to estimate attributable morbidity and mortality. Here we use data included in the Global Atlas of Helminth Infection to derive new global estimates of numbers infected with intestinal nematodes (soil-transmitted helminths, STH: Ascaris lumbricoides, Trichuris trichiura and the hookworms) and use disability-adjusted life years (DALYs) to estimate disease burden. Methods Prevalence data for 6,091 locations in 118 countries were sourced and used to estimate age-stratified mean prevalence for sub-national administrative units via a combination of model-based geostatistics (for sub-Saharan Africa) and empirical approaches (for all other regions). Geographical variation in infection prevalence within these units was approximated using modelled logit-normal distributions, and numbers of individuals with infection intensities above given thresholds estimated for each species using negative binomial distributions and age-specific worm/egg burden thresholds. Finally, age-stratified prevalence estimates for each level of infection intensity were incorporated into the Global Burden of Disease Study 2010 analytic framework to estimate the global burden of morbidity and mortality associated with each STH infection. Results Globally, an estimated 438.9 million people (95% Credible Interval (CI), 406.3 - 480.2 million) were infected with hookworm in 2010, 819.0 million (95% CI, 771.7 – 891.6 million) with A. lumbricoides and 464.6 million (95% CI, 429.6 – 508.0 million) with T. trichiura. Of the 4.98 million years lived with disability (YLDs) attributable to STH, 65% were attributable to hookworm, 22% to A. lumbricoides and the remaining 13% to T. trichiura. The vast majority of STH infections (67%) and YLDs (68%) occurred in Asia. When considering YLDs relative to total populations at risk however, the burden distribution varied more considerably within major global regions than between them. Conclusion Improvements in the cartography of helminth infection, combined with mathematical modelling approaches, have resulted in the most comprehensive contemporary estimates for the public health burden of STH. These numbers form an important benchmark upon which to evaluate future scale-up of major control efforts.
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              Population dynamics of human helminth infections: control by chemotherapy.

              An analysis is presented of the population dynamics of the major helminth parasites of man with the aim of understanding observed patterns in the age-specific prevalence and intensity of infection. Mathematical models are used to investigate the possibility of controlling helminth diseases by mass chemotherapy, and to explore the advantages of selective treatment of the most heavily infected individuals in a community.
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                Author and article information

                Contributors
                j.truscott@imperial.ac.uk
                alison.ower14@imperial.ac.uk
                m.werkman@imperial.ac.uk
                katherine.halliday@lshtm.ac.uk
                william.oswald@lshtm.ac.uk
                paulmgichuki@gmail.com
                carlos.mcharo@evidenceaction.org
                simon.brooker@gatesfoundation.org
                SNjenga@kemri.org
                mwandawirocharles@gmail.com
                walson@uw.edu
                Rachel.pullan@lshtm.ac.uk
                roy.anderson@imperial.ac.uk
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                16 September 2019
                16 September 2019
                2019
                : 12
                : 442
                Affiliations
                [1 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, London Centre for Neglected Tropical Disease Research, Department of Infectious Disease Epidemiology, , Imperial College London, ; St Mary’s Campus, London, W2 1PG UK
                [2 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, MRC Centre for Global Infectious Disease Analysis, , Imperial College London, ; St Mary’s Campus, London, W2 1PG UK
                [3 ]ISNI 0000 0001 2270 9879, GRID grid.35937.3b, The DeWorm3 Project, , The Natural History Museum, ; London, SW7 5BD UK
                [4 ]ISNI 0000 0004 0425 469X, GRID grid.8991.9, Faculty of Infectious and Tropical Diseases, , London School of Hygiene & Tropical Medicine, ; London, WC1E 7HT UK
                [5 ]ISNI 0000 0001 0155 5938, GRID grid.33058.3d, Eastern & Southern Africa Centre of International Parasite Control (ESACIPAC), , Kenya Medical Research Institute (KEMRI), ; Nairobi, Kenya
                [6 ]ISNI 0000 0000 8990 8592, GRID grid.418309.7, Bill & Melinda Gates Foundation, ; Seattle, WA USA
                [7 ]ISNI 0000000122986657, GRID grid.34477.33, Departments of Global Health, Medicine (Infectious Disease), Pediatrics and Epidemiology, , University of Washington, ; Seattle, USA
                Article
                3686
                10.1186/s13071-019-3686-2
                6745791
                31522687
                1c7a1d4f-8fcc-4b60-8251-f029a3d3fa24
                © The Author(s) 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 8 May 2019
                : 26 August 2019
                Funding
                Funded by: FundRef http://data.crossref.org/fundingdata/funder/10.13039/100000865, Bill & Melinda Gates Foundation;
                Award ID: OPP1129535
                Funded by: Children's Investment Fund Foundation
                Award ID: R-1701-01771
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Parasitology
                soil-transmitted helminths,heterogeneity,model fitting,parasite aggregation
                Parasitology
                soil-transmitted helminths, heterogeneity, model fitting, parasite aggregation

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