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Characterization of the Infectious Reservoir of Malaria with an Agent Gerardin et al. Malaria Journal (2015) 14:231 DOI 10.1186/s12936-015-0751-y RESEARCH Open Access Characterization of the infectious reservoir of malaria with an agent-based model calibrated to age-stratified parasite densities and infectiousness Jaline Gerardin1*, André Lin Ouédraogo1,2, Kevin A McCarthy1, Philip A Eckhoff1 and Edward A Wenger1 Abstract Background: Elimination of malaria can only be achieved through removal of all vectors or complete depletion of the infectious reservoir in humans. Mechanistic models can be built to synthesize diverse observations from the field collected under a variety of conditions and subsequently used to query the infectious reservoir in great detail. Methods: The EMOD model of malaria transmission was calibrated to prevalence, incidence, asexual parasite density, gametocyte density, infection duration, and infectiousness data from nine study sites. The infectious reservoir was characterized by age and parasite detectability with diagnostics of varying sensitivity over a range of transmission intensities with and without case management and vector control. Mass screen-and-treat drug campaigns were tested for likelihood of achieving elimination. Results: The composition of the infectious reservoir is similar over a range of transmission intensities, and higher intensity settings are biased towards infections in children. Recent ramp-ups in case management and use of insecticide-treated bed nets (ITNs) reduce the infectious reservoir and shift the composition towards sub-microscopic infections. Mass campaigns with anti-malarial drugs are highly effective at interrupting transmission if deployed shortly after ITN campaigns. Conclusions: Low-density infections comprise a substantial portion of the infectious reservoir. Proper timing of vector control, seasonal variation in transmission intensity and mass drug campaigns allows lingering population immunity to help drive a region towards elimination. Keywords: Mechanistic model, Infectious reservoir, Diagnostics, Infectivity, Drug campaigns Background Elimination of malaria requires interrupting transmis- Malaria is a global disease responsible for hundreds of sion. Complete depletion of the infectious reservoir of thousands of deaths each year [1]. In the last decade, malaria parasites requires clearing all malaria infections many regions have made considerable progress in malaria in both human and vector populations. In regions where control and are now working towards local elimination of malaria is endemic, accumulated exposure to infection malaria [2, 3]. Technical strategies for elimination differ leads individuals to develop immunity to clinical symp- from those for control, and it is critical to understand the toms and partial immunity to parasites. Proper identi- factors that lead to successful outcomes and make the best fication of parasite carriers is therefore confounded by use of available resources. apopulationofasymptomaticpeoplewithlow-density infections. Current rapid diagnostic tests (RDT) can quickly and cheaply identify individuals with parasite densities above * Correspondence: [email protected] 1Institute for Disease Modeling, Intellectual Ventures, 1555 132nd Ave NE, 50–200 parasites per μL [4]. However, in endemic areas, a Bellevue, WA 98005, USA significant portion of the population harbours infections Full list of author information is available at the end of the article © 2015 Gerardin et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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. Gerardin et al. Malaria Journal (2015) 14:231 Page 2 of 13 that are undetectable by RDT, and gold-standard micros- to best capture the age-dependent distribution of asexual copy or molecular methods, both limited to research parasite and gametocyte densities. Next, oocyst positivity laboratories, are required to identify infected individ- from the membrane feeding data was used to calibrate uals. Although capable of detecting infections as low model parameters governing human infectiousness to mos- as 0.01-0.05 parasites per μL, even the most sensitive quitoes. The calibrated model was then used to characterize molecular tests today cannot detect all infections [5]. the composition of the infectious reservoir by detection Asexual parasite density, gametocyte density and human threshold and age group through seasonal variations and at infectiousness are known to be linked [6, 7]. Higher asex- a range of transmission intensities. Changes in the infectious ual densities lead to higher gametocyte densities, which reservoir after deployment of case management and vector increase the chance of infecting mosquitoes. However, the control are described. Finally, the implications for elimin- relationship between gametocyte density and infectious- ation campaigns are discussedbytestinghowmassdrug ness to mosquitoes is complex, as individuals with high campaigns may successfully achieve elimination by targeting gametocyte density may infect few or no mosquitoes in all or only a portion of the infectious reservoir. studies where captured mosquitoes are fed on human blood, and individuals with no observable gametocytes Methods have been observed to be infectious [8, 9]. Human sexual- Malaria transmission model stage and transmission-blocking immunity have been pro- All simulations were conducted with EMOD DTK v1.6, posed to play roles in moderating the relationship between an agent-based mechanistic model of malaria transmission gametocyte density and infectiousness [10], but the mag- [15]. During the blood stage of malaria infection, asexual nitude and duration of sexual stage immunity effects parasite density triggers innate and adaptive immunity remain unclear. within the host. Innate immunity stimulates cytokine pro- While most malaria infections in areas of even moder- duction, leading to fever in a density-dependent manner ate transmission are asymptomatic [11], the relative con- and limiting the maximum parasite density. Adaptive tribution to the infectious reservoir of symptomatic and immunity is modelled using three types of antigens: asymptomatic, patent and sub-patent, and adult and child Plasmodium falciparum erythrocyte membrane protein populations remains an area of active investigation [12, 13]. 1 (PfEMP1) variants, merozoite surface proteins (MSP), Sub-patent individuals, even if they outnumber patent indi- and minor epitope variants. Fuller discussion of immune viduals, are less infectious to mosquitoes. In an elimination system modelling within the EMOD model is described in setting, it is critical to understand how success may or [16–18]. Asexual parasite and gametocyte densities are may not depend on appropriate targeting of sub-patent tracked within each host. Gametocytes differentiate from infections, as sensitive diagnostics can be very resource- infected red blood cells and mature in five stages over ten intensive. days, and a fraction of gametocytes are lost at each stage Mathematical modelling of malaria transmission and of maturation from implicit immune effects. Mature stage immunity can begin to answer some of these questions gametocytes are taken up in a mosquito blood meal with [12, 13]. A single mechanistic model can tie together density-dependent probability, and human and mosquito apparently contradictory field data that describe malaria immune factors implicitly limit gametocyte survival within transmission in a variety of settings and demographic the mosquito. Left untreated, all asexual and gametocyte groups. With a detailed model of within-host infection, stage parasites will eventually be cleared by host immune including parasite and gametocyte life cycles and dens- factors. Infectiousness of an individual human is calcu- ities as well as acquired immunity, the relative contribu- lated as a xenodiagnostic experiment measuring the frac- tion to the infectious reservoir due to each sub-set of the tion of mosquitoes infected after feeding on the individual. population can be compared and implications for control and elimination can be quantitatively assessed. Calibration of asexual parasite and gametocyte densities A recent longitudinal study in a high-transmission area by age and season of Burkina Faso used highly sensitive molecular detection Calibration of parasite densities built on previous work methods to quantify asexual and gametocyte densities, in [19]. Data from nine study sites were used, including providing invaluable data for model calibration [14] ethics four sites with age-stratified prevalence data: Namawala approval No. 2007-035/MS/MESSRS/CERS and 2014-0058/ in Tanzania and Matsari, Rafin Marke and Sugungum in MS/MERSI/CERS. This study also measured infectiousness Nigeria, and two sites with age-stratified clinical incidence to mosquitoes with membrane feeding tests where 50 mos- data: Dielmo and Ndiop in Senegal, that span annual ento- quitoes were fed on blood from each study participant and mological inoculation rates (EIRs) between 18 and over subsequently dissected to determine oocyst counts. Using 300 and have been used in previous work [20–23]. Re- this dataset and an agent-based stochastic model of malaria cently available
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