Heterogeneity in Transmission Parameters of Hookworm Infection Within the Baseline Data from the TUMIKIA Study in Kenya James E

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Heterogeneity in Transmission Parameters of Hookworm Infection Within the Baseline Data from the TUMIKIA Study in Kenya James E Truscott et al. Parasites Vectors (2019) 12:442 https://doi.org/10.1186/s13071-019-3686-2 Parasites & Vectors RESEARCH Open Access Heterogeneity in transmission parameters of hookworm infection within the baseline data from the TUMIKIA study in Kenya James E. Truscott1,2,3*, Alison K. Ower1,2, Marleen Werkman1,2,3, Katherine Halliday3,4, William E. Oswald3,4, Paul M. Gichuki5, Carlos Mcharo5, Simon Brooker6, Sammy M. Njenga5, Charles Mwandariwo5, Judd L. Walson1,3,7, Rachel Pullan4 and Roy Anderson1,2,3 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 efects 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 esti- mated these parameters and their variability across 120 population clusters in the study region, using a simple para- site transmission model and Gibbs-sampling Monte Carlo Markov chain techniques. We observed great heterogeneity in R0 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 fnding of this study is the increasing trend for greater parasite aggregation as prevalence declines to low levels, refected 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 moni- toring and evaluation of community infection status may need to be adapted as transmission elimination is aimed for by targeted treatment approaches. Keywords: Soil-transmitted helminths, Heterogeneity, Model ftting, Parasite aggregation Background (Ascaris lumbricoides) and hookworm (Ancylostoma Soil-transmitted helminths (STH) are the most preva- duodenale and Necator americanus), but the majority of lent of the neglected tropical diseases (NTD), infect- the global health burden results from hookworm species, ing up to 1.5 billion people world-wide. Te STH group which are estimated to account for the loss of approxi- comprises whipworm (Trichuris trichiura), roundworm mately 5.2 million disability-adjusted life years [1]. Te current WHO approach is to achieve control of STH *Correspondence: [email protected] infections through programmes of mass drug adminis- 1 London Centre for Neglected Tropical Disease Research, Department tration (MDA) targeted at school-aged and pre-school- of Infectious Disease Epidemiology, Imperial College London, St Mary’s aged children as well as other high-risk groups [2]. Campus, London W2 1PG, UK Full list of author information is available at the end of the article Recently, however, there has been an increased interest © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/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. Truscott et al. Parasites Vectors (2019) 12:442 Page 2 of 13 in the possibility of interrupting transmission through a parasite populations cannot persist due to low mating short period of intensifed community-wide MDA. Sev- success. Treshold values are strongly dependent on the eral recent and ongoing studies are currently testing this degree of parasite aggregation and transmission intensity, hypothesis [3, 4]. as measured by R0 [16, 17]. For soil-transmitted helminths, both prevalence and Based on the models that describe parasite transmis- intensity are key epidemiological measures of community sion, we can associate observed prevalence and intensity infection status for policy and programmatic decision- levels with the parameters that quantify the transmission making. Within WHO guidelines, prevalence determines cycle of the parasite and the diagnostic techniques used whether treatment is given, at what frequency and for to measure the epidemiological quantities of prevalence how long [2, 5]. Severity of infection, as measured by and intensity of infection. By ftting the model to data on the faecal egg count of infected individuals, is used as a prevalence and intensity of infection to all clusters inde- proxy for worm load and infection-induced morbidity. pendently, we can examine the variability in parameter Te latter is a key element in cost efectiveness calcula- values to see how much can be explained by cluster-level tions [6–8]. However, within larger geographical regions, environmental and demographic correlates. Importantly, a great deal of heterogeneity is observed in the meas- a model ftted to data in this way can then be applied to ured prevalence and intensity of STH infection. Tis may directly investigating how prevalence and intensity in the refect variations in environmental conditions such as region will evolve with time in individual clusters under temperature and humidity, diferences in social mixing diferent regimes of MDA treatment. or hygiene practices within the human host population, or the impacts of difering past MDA coverages [9, 10]. Methods Spatial heterogeneity in prevalence and intensity makes Epidemiological data it hard to predict how a region will respond to a control Te TUMIKIA trial was initiated in 2015 with the aim of or elimination intervention based on MDA or WASH evaluating school versus community-based deworming (water, sanitation and hygiene) improvements. As most on STH transmission in Kwale county, coastal Kenya [3, countries enter a stage of high MDA coverage, at least in 18]. Te study comprises three arms; namely, a control pre-school-aged and school-aged children, understand- group of annual school-based de-worming, a group with ing the efects of MDA on STH infections is a prereq- annual community-wide deworming, and a third group uisite for the evaluation of the possible interruption of with community-wide deworming biannually. Te data parasite transmission at the community level. used in this analysis comes from the baseline survey. Tis study analyses the spatial variability in hookworm In the decade prior to the baseline survey of the study, prevalence and intensity in a collection of contiguous this region received several rounds of lymphatic flariasis communities taken from the baseline of a cluster-ran- (LF) treatment (in 2003, 2005, 2008 and 2011), employ- domized trial conducted in coastal Kenya to evaluate ing diethylcarbamazine citrate (DEC, 6 mg/kg) plus treatment strategies for the soil transmitted helminths albendazole (400 mg), through the National Programme [3]. We seek to characterize the variability in the preva- for Elimination of Lymphatic Filariasis (NPELF) [19]. lence and intensity in terms of key epidemiological Furthermore, from 2012 through 2014 annual school- parameters, such as the basic reproduction number (R0) based deworming with albendazole (400 mg) occurred and the degree of parasite aggregation (as measured through a programme, run by the Kenyan Ministries of inversely by the negative binomial parameter k) in the Health and Education, to deworm all school-aged and human host population. Te analysis is based on ftting a pre-school-aged children living in high STH risk areas disease transmission mathematical model to the baseline [20]. However, there is strong anecdotal evidence that the data. Tis approach ensures that the resulting param- efective coverage levels for the prior rounds of treatment eter values refect the disease transmission processes are signifcantly lower than those ofcially recorded (per- found in endemic (or approximately endemic) parasite haps averaging 30% in reality). populations. Te baseline survey was conducted in 120 contigu- Our method puts constraints on possible parameter ous study clusters, each comprising approximately 1000 fts that are not present in purely statistical approaches to households or 5000 individuals. We used the cross-sec- analyses [11–14]. Mathematical models of macroparasite tional hookworm data from the study baseline, deter- infection predict ‘breakpoints’ in transmission created by mined using duplicate Kato-Katz slide readings from a the dioecious nature of helminths and the concomitant single stool sample. Sample sizes from clusters ranged need for both male and female parasites to be in the same from 110 to 294 individuals of all ages, selected
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