Publications
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Sherrard-Smith E, Skarp JE, Beale AD, et al., 2019, Mosquito feeding behavior and how it influences residual malaria transmission across Africa, Proceedings of the National Academy of Sciences, Vol: 116, Pages: 15086-15095, ISSN: 0027-8424
The antimalarial efficacy of the most important vector control interventions—long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS)—primarily protect against mosquitoes’ biting people when they are in bed and indoors. Mosquito bites taken outside of these times contribute to residual transmission which determines the maximum effectiveness of current malaria prevention. The likelihood mosquitoes feed outside the time of day when LLINs and IRS can protect people is poorly understood, and the proportion of bites received outdoors may be higher after prolonged vector control. A systematic review of mosquito and human behavior is used to quantify and estimate the public health impact of outdoor biting across Africa. On average 79% of bites by the major malaria vectors occur during the time when people are in bed. This estimate is substantially lower than previous predictions, with results suggesting a nearly 10% lower proportion of bites taken at the time when people are beneath LLINs since the year 2000. Across Africa, this higher outdoor transmission is predicted to result in an estimated 10.6 million additional malaria cases annually if universal LLIN and IRS coverage was achieved. Higher outdoor biting diminishes the cases of malaria averted by vector control. This reduction in LLIN effectiveness appears to be exacerbated in areas where mosquito populations are resistant to insecticides used in bed nets, but no association was found between physiological resistance and outdoor biting. Substantial spatial heterogeneity in mosquito biting behavior between communities could contribute to differences in effectiveness of malaria control across Africa.
Dixon MA, Braae UC, Winskill P, et al., 2019, Strategies for tackling Taenia solium taeniosis/cysticercosis: A systematic review and comparison of transmission models, including an assessment of the wider Taeniidae family transmission models, PLoS Neglected Tropical Diseases, Vol: 13, ISSN: 1935-2727
BackgroundThe cestode Taenia solium causes the neglected (zoonotic) tropical disease cysticercosis, a leading cause of preventable epilepsy in endemic low and middle-income countries. Transmission models can inform current scaling-up of control efforts by helping to identify, validate and optimise control and elimination strategies as proposed by the World Health Organization (WHO).Methodology/Principal findingsA systematic literature search was conducted using the PRISMA approach to identify and compare existing T. solium transmission models, and related Taeniidae infection transmission models. In total, 28 modelling papers were identified, of which four modelled T. solium exclusively. Different modelling approaches for T. solium included deterministic, Reed-Frost, individual-based, decision-tree, and conceptual frameworks. Simulated interventions across models agreed on the importance of coverage for impactful effectiveness to be achieved.Other Taeniidae infection transmission models comprised force-of-infection (FoI), population-based (mainly Echinococcus granulosus) and individual-based (mainly E. multilocularis) modelling approaches. Spatial structure has also been incorporated (E. multilocularis and Taenia ovis) in recognition of spatial aggregation of parasite eggs in the environment and movement of wild animal host populations.Conclusions/SignificanceGaps identified from examining the wider Taeniidae family models highlighted the potential role of FoI modelling to inform model parameterisation, as well as the need for spatial modelling and suitable structuring of interventions as key areas for future T. solium model development. We conclude that working with field partners to address data gaps and conducting cross-model validation with baseline and longitudinal data will be critical to building consensus-led and epidemiological setting-appropriate intervention strategies to help fulfil the WHO targets.
Winskill P, Walker PG, Cibulskis RE, et al., 2019, Prioritizing the scale-up of interventions for malaria control and elimination, Malaria Journal, Vol: 18, ISSN: 1475-2875
BackgroundA core set of intervention and treatment options are recommended by the World Health Organization for use against falciparum malaria. These are treatment, long-lasting insecticide-treated bed nets, indoor residual spraying, and chemoprevention options. Both domestic and foreign aid funding for these tools is limited. When faced with budget restrictions, the introduction and scale-up of intervention and treatment options must be prioritized.MethodsEstimates of the cost and impact of different interventions were combined with a mathematical model of malaria transmission to estimate the most cost-effective prioritization of interventions. The incremental cost effectiveness ratio was used to select between scaling coverage of current interventions or the introduction of an additional intervention tool.ResultsPrevention, in the form of vector control, is highly cost effective and scale-up is prioritized in all scenarios. Prevention reduces malaria burden and therefore allows treatment to be implemented in a more cost-effective manner by reducing the strain on the health system. The chemoprevention measures (seasonal malaria chemoprevention and intermittent preventive treatment in infants) are additional tools that, provided sufficient funding, are implemented alongside treatment scale-up. Future tools, such as RTS,S vaccine, have impact in areas of higher transmission but were introduced later than core interventions.ConclusionsIn a programme that is budget restricted, it is essential that investment in available tools be effectively prioritized to maximize impact for a given investment. The cornerstones of malaria control: vector control and treatment, remain vital, but questions of when to scale and when to introduce other interventions must be rigorously assessed. This quantitative analysis considers the scale-up or core interventions to inform decision making in this area.
Winskill P, Walker P, Cibulskis R, et al., 2019, Prioritizing the scale up of interventions for malaria control and elimination, Malaria Journal, ISSN: 1475-2875
Winskill P, Lambert B, Hogan AB, et al., 2019, INEQUITIES IN THE BURDEN OF FEVER, DIARRHEA AND ACUTE RESPIRATORY INFECTION IN CHILDREN UNDER FIVE IN LOW- AND MIDDLE-INCOME COUNTRIES AND THE ROLE OF INTEGRATED COMMUNITY CASE MANAGEMENT IN TARGETING THOSE MOST AT RISK, 68th Annual Meeting of the American-Society-for-Tropical-Medicine-and-Hygiene (ASTMH)
Sherrard-Smith E, Griffin J, Winskill P, et al., 2018, Systematic review of indoor residual spray efficacy and effectiveness against Plasmodium falciparum in Africa, Nature Communications, Vol: 9, ISSN: 2041-1723
Indoor residual spraying (IRS) is an important part of malaria control. There is a growing list of insecticide classes; pyrethroids remain the principal insecticide used in bednets but recently, novel non-pyrethroid IRS products, with contrasting impacts, have been introduced. There is an urgent need to better assess product efficacy to help decision makers choose effective and relevant tools for mosquito control. Here we use experimental hut trial data to characterise the entomological efficacy of widely-used, novel IRS insecticides. We quantify their impact against pyrethroid-resistant mosquitoes and use a Plasmodium falciparum transmission model to predict the public health impact of different IRS insecticides. We report that long-lasting IRS formulations substantially reduce malaria, though their benefit over cheaper, shorter-lived formulations depends on local factors including bednet use, seasonality, endemicity and pyrethroid resistance status of local mosquito populations. We provide a framework to help decision makers evaluate IRS product effectiveness.
Hogan A, Winskill P, Verity R, et al., 2018, Informing target product profiles for a second-generation childhood malaria vaccine: a modelling study, 67th Annual Meeting of the American-Society-of-Tropical-Medicine-and-Hygiene (ASTHM), Publisher: AMER SOC TROP MED & HYGIENE, Pages: 583-583, ISSN: 0002-9637
Hogan AB, Winskill P, Verity R, et al., 2018, Modelling population-level impact to inform target product profiles for childhood malaria vaccines, BMC Medicine, Vol: 16, ISSN: 1741-7015
BackgroundThe RTS,S/AS01 vaccine for Plasmodium falciparum malaria demonstrated moderate efficacy in 5–17-month-old children in phase 3 trials, and from 2018, the vaccine will be evaluated through a large-scale pilot implementation program. Work is ongoing to optimise this vaccine, with higher efficacy for a different schedule demonstrated in a phase 2a challenge study. The objective of our study was to investigate the population-level impact of a modified RTS,S/AS01 schedule and dose amount in order to inform the target product profile for a second-generation malaria vaccine.MethodsWe used a mathematical modelling approach as the basis for our study. We simulated the changing anti-circumsporozoite antibody titre following vaccination and related the titre to vaccine efficacy. We then implemented this efficacy profile within an individual-based model of malaria transmission. We compared initial efficacy, duration and dose timing, and evaluated the potential public health impact of a modified vaccine in children aged 5–17 months, measuring clinical cases averted in children younger than 5 years.ResultsIn the first decade of delivery, initial efficacy was associated with a higher reduction in childhood clinical cases compared to vaccine duration. This effect was more pronounced in high transmission settings and was due to the efficacy benefit occurring in younger ages where disease burden is highest. However, the low initial efficacy and long duration schedule averted more cases across all age cohorts if a longer time horizon was considered. We observed an age-shifting effect due to the changing immunological profile in higher transmission settings, in scenarios where initial efficacy was higher, and the fourth dose administered earlier.ConclusionsOur findings indicate that, for an imperfect childhood malaria vaccine with suboptimal efficacy, it may be advantageous to prioritise initial efficacy over duration. We predict that a modified vaccine could outpe
Robinson A, Busula AO, Voets MA, et al., 2018, Plasmodium-associated changes in human odor attract mosquitoes, Proceedings of the National Academy of Sciences, Vol: 115, Pages: E4209-E4218, ISSN: 0027-8424
Malaria parasites (Plasmodium) can change the attractiveness of their vertebrate hosts to Anopheles vectors, leading to a greater number of vector-host contacts and increased transmission. Indeed, naturally Plasmodium-infected children have been shown to attract more mosquitoes than parasite-free children. Here, we demonstrate Plasmodium-induced increases in the attractiveness of skin odor in Kenyan children, and reveal quantitative differences in the production of specific odor components in infected, versus parasite-free, individuals. We found the aldehydes heptanal, octanal and nonanal to be produced in greater amounts by infected individuals, and detected by mosquito antennae. In behavioral experiments, we demonstrated that these, and other, Plasmodium-induced aldehydes enhanced the attractiveness of a synthetic odor blend mimicking ‘healthy’ human odor. Heptanal alone increased the attractiveness of ‘parasite-free’ natural human odor. Should the increased production of these aldehydes by Plasmodium-infected humans lead to increased mosquito biting in a natural setting, this would likely affect the transmission of malaria.
Dixon M, Braae U, Winskill P, et al., 2018, TOWARDS THE DESIGN AND OPTIMIZATION OF INTERVENTION STRATEGIES AGAINST <it>TAENIA SOLIUM</it> TAENIOSIS/CYSTICERCOSIS BY MULTI-MODEL COMPARISON, 67th Annual Meeting of the American-Society-of-Tropical-Medicine-and-Hygiene (ASTHM), Publisher: AMER SOC TROP MED & HYGIENE, Pages: 151-151, ISSN: 0002-9637
Winskill P, Slater H, Griffin J, et al., 2017, The US President's Malaria Initiative, Plasmodium falciparum transmission and mortality: A modelling study, PLoS Medicine, Vol: 14, ISSN: 1549-1277
BackgroundAlthough significant progress has been made in reducing malaria transmission globally inrecent years, a large number of people remain at risk and hence the gains made are fragile.Funding lags well behind amounts needed to protect all those at risk and ongoing contributionsfrom major donors, such as the President’s Malaria Initiative (PMI), are vital to maintainprogress and pursue further reductions in burden. We use a mathematical modellingapproach to estimate the impact of PMI investments to date in reducing malaria burden andto explore the potential negative impact on malaria burden should a proposed 44% reductionin PMI funding occur.Methods and findingsWe combined an established mathematical model of Plasmodium falciparum transmissiondynamics with epidemiological, intervention, and PMI-financing data to estimate the contributionPMI has made to malaria control via funding for long-lasting insecticide treated nets(LLINs), indoor residual spraying (IRS), and artemisinin combination therapies (ACTs). Weestimate that PMI has prevented 185 million (95% CrI: 138 million, 230 million) malariacases and saved 940,049 (95% CrI: 545,228, 1.4 million) lives since 2005. If funding is maintained,PMI-funded interventions are estimated to avert a further 162 million cases (95%CrI: 116 million, 194 million) cases, saving a further 692,589 (95% CrI: 392,694, 955,653)lives between 2017 and 2020. With an estimate of US$94 (95% CrI: US$51, US$166) perDisability Adjusted Life Year (DALY) averted, PMI-funded interventions are highly costeffective.We also demonstrate the further impact of this investment by reducing caseloadson health systems. If a 44% reduction in PMI funding were to occur, we predict that this lossof direct aid could result in an additional 67 million (95% CrI: 49 million, 82 million) cases and290,649 deaths (95% CrI: 167,208, 395,263) deaths between 2017 and 2020. We have notmodelled indirect impacts of PMI funding (such as health systems strengthening
Winskill P, Walker PG, Griffin JT, et al., 2017, OPTIMIZING THE GLOBAL ALLOCATION OF MALARIA FUNDS, 65th Annual Meeting of the American-Society-of-Tropical-Medicine-and-Hygiene (ASTMH), Publisher: AMER SOC TROP MED & HYGIENE, Pages: 117-117, ISSN: 0002-9637
Winskill P, Harrison W, French M, et al., 2017, Assessing the impact of intervention strategies against Taenia solium cysticercosis using the EPICYST transmission model, Parasites & Vectors, Vol: 10, ISSN: 1756-3305
BackgroundThe pork tapeworm, Taenia solium, and associated human infections, taeniasis, cysticercosis and neurocysticercosis, are serious public health problems, especially in developing countries. The World Health Organization (WHO) has set goals for having a validated strategy for control and elimination of T. solium taeniasis/cysticercosis by 2015 and interventions scaled-up in selected countries by 2020. Timely achievement of these internationally-endorsed targets requires that the relative benefits and effectiveness of potential interventions be explored rigorously within a quantitative framework.MethodsA deterministic, compartmental transmission model (EPICYST) was developed to capture the dynamics of the taeniasis/cysticercosis disease system in the human and pig hosts. Cysticercosis prevalence in humans, an outcome of high epidemiological and clinical importance, was explicitly modelled. A next generation matrix approach was used to derive an expression for the basic reproduction number, R 0. A full sensitivity analysis was performed using a methodology based on Latin-hypercube sampling partial rank correlation coefficient index.ResultsEPICYST outputs indicate that chemotherapeutic intervention targeted at humans or pigs would be highly effective at reducing taeniasis and cysticercosis prevalence when applied singly, with annual chemotherapy of humans and pigs resulting, respectively, in 94 and 74% of human cysticercosis cases averted. Improved sanitation, meat inspection and animal husbandry are less effective but are still able to reduce prevalence singly or in combination. The value of R 0 for taeniasis was estimated at 1.4 (95% Credible Interval: 0.5–3.6).ConclusionsHuman- and pig-targeted drug-focussed interventions appear to be the most efficacious approach from the options currently available. The model presented is a forward step towards developing an informed control and elimination strategy for cysticercosis. Together with its validation agai
Winskill P, Walker P, Griffin J, et al., 2017, Modelling the cost-effectiveness of introducing the RTS,S malaria vaccine relative to scaling up other malaria interventions in sub-Saharan Africa, BMJ Global Health, Vol: 2, ISSN: 2059-7908
Objectives: To evaluate the relative cost-effectiveness of introducing the RTS,S malaria vaccine in sub-Saharan Africa compared with further scale-up of existing interventions.Design: A mathematical modelling and cost-effectiveness study.Setting: Sub-Saharan Africa.Participants: People of all ages.Interventions: The analysis considers the introduction and scale-up of the RTS,S malaria vaccine and the scale-up of long lasting insecticide treated bed nets (LLINs), indoor residual spraying (IRS) and seasonal malaria chemoprevention (SMC).Main outcome measure: The number of Plasmodium falciparum cases averted in all age groups over a ten year period.Results: Assuming access to treatment remains constant, increasing coverage of LLINs was consistently the most cost-effective intervention across a range of transmission settings and was found to occur early in the cost-effectiveness scale-up pathway. IRS, RTS,S and SMC entered the cost-effective pathway once LLIN coverage had been maximised. If non-linear production functions are included to capture the cost of reaching very high coverage, the resulting pathways become more complex and result in selection of multiple interventions.Conclusions: RTS,S was consistently implemented later in the cost-effectiveness pathway than the LLINs, IRS and SMC but was still of value as a fourth intervention in many settings to reduce burden to the levels set out in the international goals.
Winskill P, Slater HC, Griffin JT, et al., 2017, THE IMPORTANCE OF US FOREIGN AID FOR GLOBAL MALARIA CONTROL AND ELIMINATION, 66th Annual Meeting of the American-Society-of-Tropical-Medicine-and-Hygiene (ASTMH), Publisher: AMER SOC TROP MED & HYGIENE, Pages: 217-217, ISSN: 0002-9637
Sherrard-Smith E, Winskill P, Griffin JT, et al., 2017, A SYSTEMATIC REVIEW OF INDOOR RESIDUAL SPRAYING TO INVESTIGATE THE IMPACT OF PYRETHROID RESISTANCE ON MALARIA TRANSMISSION, 66th Annual Meeting of the American-Society-of-Tropical-Medicine-and-Hygiene (ASTMH), Publisher: AMER SOC TROP MED & HYGIENE, Pages: 137-137, ISSN: 0002-9637
Basanez M, Lamberton PHL, Cheke RA, et al., 2016, Onchocerciasis transmission in Ghana: the human blood index of sibling species of the Simulium damnosum complex, Parasites & Vectors, Vol: 9, ISSN: 1756-3305
BackgroundVector-biting behaviour is important for vector-borne disease (VBD) epidemiology. The proportion of blood meals taken on humans (the human blood index, HBI), is a component of the biting rate per vector on humans in VBD transmission models. Humans are the definitive host of Onchocerca volvulus, but the simuliid vectors feed on a range of animals and HBI is a key indicator of the potential for human onchocerciasis transmission. Ghana has a diversity of Simulium damnosum complex members, which are likely to vary in their HBIs, an important consideration for parameterization of onchocerciasis control and elimination models.MethodsHost-seeking and ovipositing S. damnosum (sensu lato) (s.l.) were collected from seven villages in four Ghanaian regions. Taxa were morphologically and molecularly identified. Blood meals from individually stored blackfly abdomens were used for DNA profiling, to identify previous host choice. Household, domestic animal, wild mammal and bird surveys were performed to estimate the density and diversity of potential blood hosts of blackflies.ResultsA total of 11,107 abdomens of simuliid females (which would have obtained blood meal(s) previously) were tested, with blood meals successfully amplified in 3,772 (34 %). A single-host species was identified in 2,857 (75.7 %) of the blood meals, of which 2,162 (75.7 %) were human. Simulium soubrense Beffa form, S. squamosum C and S. sanctipauli Pra form were the most anthropophagic (HBI = 0.92, 0.86 and 0.70, respectively); S. squamosum E, S. yahense and S. damnosum (sensu stricto) (s.s.)/S. sirbanum were the most zoophagic (HBI = 0.44, 0.53 and 0.63, respectively). The degree of anthropophagy decreased (but not statistically significantly) with increasing ratio of non-human/human blood hosts. Vector to human ratios ranged from 139 to 1,198 blackflies/person.ConclusionsDNA profiling can successfully identify blood meals from host-seeking and ovipositing blackflies.
Winskill P, Carvalho DO, Capurro ML, et al., 2015, Dispersal of engineered male Aedes aegypti mosquitoes, PLOS Neglected Tropical Diseases, Vol: 9, ISSN: 1935-2735
BackgroundAedes aegypti, the principal vector of dengue fever, have been genetically engineered for use in a sterile insect control programme. To improve our understanding of the dispersal ecology of mosquitoes and to inform appropriate release strategies of ‘genetically sterile’ male Aedes aegypti detailed knowledge of the dispersal ability of the released insects is needed.Methodology/Principal FindingsThe dispersal ability of released ‘genetically sterile’ male Aedes aegypti at a field site in Brazil has been estimated. Dispersal kernels embedded within a generalized linear model framework were used to analyse data collected from three large scale mark release recapture studies. The methodology has been applied to previously published dispersal data to compare the dispersal ability of ‘genetically sterile’ male Aedes aegypti in contrasting environments. We parameterised dispersal kernels and estimated the mean distance travelled for insects in Brazil: 52.8m (95% CI: 49.9m, 56.8m) and Malaysia: 58.0m (95% CI: 51.1m, 71.0m).Conclusions/SignificanceOur results provide specific, detailed estimates of the dispersal characteristics of released ‘genetically sterile’ male Aedes aegypti in the field. The comparative analysis indicates that despite differing environments and recapture rates, key features of the insects’ dispersal kernels are conserved across the two studies. The results can be used to inform both risk assessments and release programmes using ‘genetically sterile’ male Aedes aegypti.Author SummaryVector control using releases of sterile insects is a well-known approach. ‘Genetically sterile’ male Aedes aegypti have been developed and released in a modern realisation of the sterile insect technique. Released engineered males seek out and mate with wild females, with the resultant offspring dying before they reach maturity. Control of a wild vector population can therefore be achiev
Winskill P, Walker PG, Griffin JT, et al., 2015, COST-EFFECTIVE SCALE-UP OF CURRENT INTERVENTIONS AND RTS,S IN SUB-SAHARAN AFRICAN SETTINGS, Publisher: AMER SOC TROP MED & HYGIENE, Pages: 477-477, ISSN: 0002-9637
Curtis Z, Matzen K, Oviedo MN, et al., 2015, Assessment of the Impact of Potential Tetracycline Exposure on the Phenotype of Aedes aegypti OX513A: Implications for Field Use, PLOS Neglected Tropical Diseases, Vol: 9, ISSN: 1935-2735
Lamberton PHL, Cheke RA, Winskill P, et al., 2015, Onchocerciasis Transmission in Ghana: Persistence under Different Control Strategies and the Role of the Simuliid Vectors, PLOS Neglected Tropical Diseases, Vol: 9, ISSN: 1935-2735
Lamberton PHL, Cheke RA, Walker M, et al., 2014, Onchocerciasis transmission in Ghana: biting and parous rates of host-seeking sibling species of the <i>Simulium damnosum</i> complex, PARASITES & VECTORS, Vol: 7, ISSN: 1756-3305
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Winskill P, Harris AF, Morgan SA, et al., 2014, Genetic control of Aedes aegypti: data-driven modelling to assess the effect of releasing different life stages and the potential for long-term suppression, Parasites & Vectors, Vol: 7, ISSN: 1756-3305
Winskill P, McKemey A, Alphey L, et al., 2013, OPTIMISING FIELD RELEASES OF ENGINEERED MALE MOSQUITOES, PATHOGENS AND GLOBAL HEALTH, Vol: 107, Pages: 421-421, ISSN: 2047-7724
Walker M, Winskill P, Basanez M-G, et al., 2013, Temporal and micro-spatial heterogeneity in the distribution of <i>Anopheles</i> vectors of malaria along the Kenyan coast, PARASITES & VECTORS, Vol: 6, ISSN: 1756-3305
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Nordin O, Donald W, Ming WH, et al., 2013, Oral Ingestion of Transgenic RIDL <i>Ae</i>. <i>aegypti</i> Larvae Has No Negative Effect on Two Predator <i>Toxorhynchites</i> Species, PLOS ONE, Vol: 8, ISSN: 1932-6203
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Winskill P, Rowland M, Mtove G, et al., 2011, Malaria risk factors in north-east Tanzania, MALARIA JOURNAL, Vol: 10, ISSN: 1475-2875
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