Modelled and observed mean and seasonal relationships between climate, population density and malaria indicators in Cameroon.

BACKGROUND: A major health burden in Cameroon is malaria, a disease that is sensitive to climate, environment and socio-economic conditions, but whose precise relationship with these drivers is still uncertain. An improved understanding of the relationship between the disease and its drivers, and the ability to represent these relationships in dynamic disease models, would allow such models to contribute to health mitigation and adaptation planning. This work collects surveys of malaria parasite ratio and entomological inoculation rate and examines their relationship with temperature, rainfall, population density in Cameroon and uses this analysis to evaluate a climate sensitive mathematical model of malaria transmission. METHODS: Co-located, climate and population data is compared to the results of 103 surveys of parasite ratio (PR) covering 18,011 people in Cameroon. A limited set of campaigns which collected year-long field-surveys of the entomological inoculation rate (EIR) are examined to determine the seasonality of disease transmission, three of the study locations are close to the Sanaga and Mefou rivers while others are not close to any permanent water feature. Climate-driven simulations of the VECTRI malaria model are evaluated with this analysis. RESULTS: The analysis of the model results shows the PR peaking at temperatures of approximately 22 °C to 26 °C, in line with recent work that has suggested a cooler peak temperature relative to the established literature, and at precipitation rates at 7 mm day-1, somewhat higher than earlier estimates. The malaria model is able to reproduce this broad behaviour, although the peak occurs at slightly higher temperatures than observed, while the PR peaks at a much lower rainfall rate of 2 mm day-1. Transmission tends to be high in rural and peri-urban relative to urban centres in both model and observations, although the model is oversensitive to population which could be due to the neglect of population movements, and differences in hydrological conditions, housing quality and access to healthcare. The EIR follows the seasonal rainfall with a lag of 1 to 2 months, and is well reproduced by the model, while in three locations near permanent rivers the annual cycle of malaria transmission is out of phase with rainfall and the model fails. CONCLUSION: Malaria prevalence is maximum at temperatures of 24 to 26 °C in Cameroon and rainfall rates of approximately 4 to 6 mm day-1. The broad relationships are reproduced in a malaria model although prevalence is highest at a lower rainfall maximum of 2 mm day-1. In locations far from water bodies malaria transmission seasonality closely follows that of rainfall with a lag of 1 to 2 months, also reproduced by the model, but in locations close to a seasonal river the seasonality of malaria transmission is reversed due to pooling in the transmission to the dry season, which the model fails to capture.

Impact of climate change on global malaria distribution.

Malaria is an important disease that has a global distribution and significant health burden. The spatial limits of its distribution and seasonal activity are sensitive to climate factors, as well as the local capacity to control the disease. Malaria is also one of the few health outcomes that has been modeled by more than one research group and can therefore facilitate the first model intercomparison for health impacts under a future with climate change. We used bias-corrected temperature and rainfall simulations from the Coupled Model Intercomparison Project Phase 5 climate models to compare the metrics of five statistical and dynamical malaria impact models for three future time periods (2030s, 2050s, and 2080s). We evaluated three malaria outcome metrics at global and regional levels: climate suitability, additional population at risk and additional person-months at risk across the model outputs. The malaria projections were based on five different global climate models, each run under four emission scenarios (Representative Concentration Pathways, RCPs) and a single population projection. We also investigated the modeling uncertainty associated with future projections of populations at risk for malaria owing to climate change. Our findings show an overall global net increase in climate suitability and a net increase in the population at risk, but with large uncertainties. The model outputs indicate a net increase in the annual person-months at risk when comparing from RCP2.6 to RCP8.5 from the 2050s to the 2080s. The malaria outcome metrics were highly sensitive to the choice of malaria impact model, especially over the epidemic fringes of the malaria distribution.

Multisectoral climate impact hotspots in a warming world.

The impacts of global climate change on different aspects of humanity's diverse life-support systems are complex and often difficult to predict. To facilitate policy decisions on mitigation and adaptation strategies, it is necessary to understand, quantify, and synthesize these climate-change impacts, taking into account their uncertainties. Crucial to these decisions is an understanding of how impacts in different sectors overlap, as overlapping impacts increase exposure, lead to interactions of impacts, and are likely to raise adaptation pressure. As a first step we develop herein a framework to study coinciding impacts and identify regional exposure hotspots. This framework can then be used as a starting point for regional case studies on vulnerability and multifaceted adaptation strategies. We consider impacts related to water, agriculture, ecosystems, and malaria at different levels of global warming. Multisectoral overlap starts to be seen robustly at a mean global warming of 3 °C above the 1980-2010 mean, with 11% of the world population subject to severe impacts in at least two of the four impact sectors at 4 °C. Despite these general conclusions, we find that uncertainty arising from the impact models is considerable, and larger than that from the climate models. In a low probability-high impact worst-case assessment, almost the whole inhabited world is at risk for multisectoral pressures. Hence, there is a pressing need for an increased research effort to develop a more comprehensive understanding of impacts, as well as for the development of policy measures under existing uncertainty.

A regional-scale, high resolution dynamical malaria model that accounts for population density, climate and surface hydrology.

BACKGROUND: The relative roles of climate variability and population related effects in malaria transmission could be better understood if regional-scale dynamical malaria models could account for these factors. METHODS: A new dynamical community malaria model is introduced that accounts for the temperature and rainfall influences on the parasite and vector life cycles which are finely resolved in order to correctly represent the delay between the rains and the malaria season. The rainfall drives a simple but physically based representation of the surface hydrology. The model accounts for the population density in the calculation of daily biting rates. RESULTS: Model simulations of entomological inoculation rate and circumsporozoite protein rate compare well to data from field studies from a wide range of locations in West Africa that encompass both seasonal endemic and epidemic fringe areas. A focus on Bobo-Dioulasso shows the ability of the model to represent the differences in transmission rates between rural and peri-urban areas in addition to the seasonality of malaria. Fine spatial resolution regional integrations for Eastern Africa reproduce the malaria atlas project (MAP) spatial distribution of the parasite ratio, and integrations for West and Eastern Africa show that the model grossly reproduces the reduction in parasite ratio as a function of population density observed in a large number of field surveys, although it underestimates malaria prevalence at high densities probably due to the neglect of population migration. CONCLUSIONS: A new dynamical community malaria model is publicly available that accounts for climate and population density to simulate malaria transmission on a regional scale. The model structure facilitates future development to incorporate migration, immunity and interventions.

Relative importance of climatic, geographic and socio-economic determinants of malaria in Malawi.

BACKGROUND: Malaria transmission is influenced by variations in meteorological conditions, which impact the biology of the parasite and its vector, but also socio-economic conditions, such as levels of urbanization, poverty and education, which impact human vulnerability and vector habitat. The many potential drivers of malaria, both extrinsic, such as climate, and intrinsic, such as population immunity are often difficult to disentangle. This presents a challenge for the modelling of malaria risk in space and time. METHODS: A statistical mixed model framework is proposed to model malaria risk at the district level in Malawi, using an age-stratified spatio-temporal dataset of malaria cases from July 2004 to June 2011. Several climatic, geographic and socio-economic factors thought to influence malaria incidence were tested in an exploratory model. In order to account for the unobserved confounding factors that influence malaria, which are not accounted for using measured covariates, a generalized linear mixed model was adopted, which included structured and unstructured spatial and temporal random effects. A hierarchical Bayesian framework using Markov chain Monte Carlo simulation was used for model fitting and prediction. RESULTS: Using a stepwise model selection procedure, several explanatory variables were identified to have significant associations with malaria including climatic, cartographic and socio-economic data. Once intervention variations, unobserved confounding factors and spatial correlation were considered in a Bayesian framework, a final model emerged with statistically significant predictor variables limited to average precipitation (quadratic relation) and average temperature during the three months previous to the month of interest. CONCLUSIONS: When modelling malaria risk in Malawi it is important to account for spatial and temporal heterogeneity and correlation between districts. Once observed and unobserved confounding factors are allowed for, precipitation and temperature in the months prior to the malaria season of interest are found to significantly determine spatial and temporal variations of malaria incidence. Climate information was found to improve the estimation of malaria relative risk in 41% of the districts in Malawi, particularly at higher altitudes where transmission is irregular. This highlights the potential value of climate-driven seasonal malaria forecasts.

Climate Drivers of Malaria Transmission Seasonality and Their Relative Importance in Sub-Saharan Africa.

A new database of the Entomological Inoculation Rate (EIR) was used to directly link the risk of infectious mosquito bites to climate in Sub-Saharan Africa. Applying a statistical mixed model framework to high-quality monthly EIR measurements collected from field campaigns in Sub-Saharan Africa, we analyzed the impact of rainfall and temperature seasonality on EIR seasonality and determined important climate drivers of malaria seasonality across varied climate settings in the region. We observed that seasonal malaria transmission was within a temperature window of 15°C-40°C and was sustained if average temperature was well above 15°C or below 40°C. Monthly maximum rainfall for seasonal malaria transmission did not exceed 600 in west Central Africa, and 400 mm in the Sahel, Guinea Savannah, and East Africa. Based on a multi-regression model approach, rainfall and temperature seasonality were found to be significantly associated with malaria seasonality in all parts of Sub-Saharan Africa except in west Central Africa. Topography was found to have significant influence on which climate variable is an important determinant of malaria seasonality in East Africa. Seasonal malaria transmission onset lags behind rainfall only at markedly seasonal rainfall areas such as Sahel and East Africa; elsewhere, malaria transmission is year-round. High-quality EIR measurements can usefully supplement established metrics for seasonal malaria. The study's outcome is important for the improvement and validation of weather-driven dynamical mathematical malaria models that directly simulate EIR. Our results can contribute to the development of fit-for-purpose weather-driven malaria models to support health decision-making in the fight to control or eliminate malaria in Sub-Saharan Africa.

Impact of a Mixed Ocean Layer and the Diurnal Cycle on Convective Aggregation.

We investigate how ocean feedbacks and the diurnal cycle impact convective aggregation using a slab ocean coupled to a cloud resolving model. With a 20 m mixed layer ocean, aggregation occurs after 25 days. Thinner ocean layers slow the onset of clustering, with a 1 m ocean layer needing around 43 days. The delay is due to anomalous solar radiation in clear sky regions, causing a relative surface warming balanced by a matching cooling in cloudy areas. The resulting gradient in surface heat fluxes opposes low level convergence into convecting regions. On aggregation, the convective regions are surrounded by moist, clear sky regions with the hottest SSTs, toward which convection migrates, while a cold SST patch forms under dry suppressed regions due to enhanced latent heat fluxes and longwave radiation. The next experiment allows a diurnal cycle of 2.5°C in the domain mean SST. This causes convective rainfall to shift from a weak morning maximum to a sharper evening peak, reminiscent of undisturbed tropical observations. However, convection reverts to a weak early morning maximum once aggregation starts due to spatially heterogeneous radiative forcing. This implies thin mixed ocean layers are a necessary but non-sufficient condition for an afternoon maximum of convection; limited spatial water vapor variability is also necessary. The imposition of the mean diurnal cycle has no statistically significant impact on the mean timing of clustering onset.

Impact of an accelerated melting of Greenland on malaria distribution over Africa.

Studies about the impact of future climate change on diseases have mostly focused on standard Representative Concentration Pathway climate change scenarios. These scenarios do not account for the non-linear dynamics of the climate system. A rapid ice-sheet melting could occur, impacting climate and consequently societies. Here, we investigate the additional impact of a rapid ice-sheet melting of Greenland on climate and malaria transmission in Africa using several malaria models driven by Institute Pierre Simon Laplace climate simulations. Results reveal that our melting scenario could moderate the simulated increase in malaria risk over East Africa, due to cooling and drying effects, cause a largest decrease in malaria transmission risk over West Africa and drive malaria emergence in southern Africa associated with a significant southward shift of the African rain-belt. We argue that the effect of such ice-sheet melting should be investigated further in future public health and agriculture climate change risk assessments.

Projecting the risk of mosquito-borne diseases in a warmer and more populated world: a multi-model, multi-scenario intercomparison modelling study.

BACKGROUND: Mosquito-borne diseases are expanding their range, and re-emerging in areas where they had subsided for decades. The extent to which climate change influences the transmission suitability and population at risk of mosquito-borne diseases across different altitudes and population densities has not been investigated. The aim of this study was to quantify the extent to which climate change will influence the length of the transmission season and estimate the population at risk of mosquito-borne diseases in the future, given different population densities across an altitudinal gradient. METHODS: Using a multi-model multi-scenario framework, we estimated changes in the length of the transmission season and global population at risk of malaria and dengue for different altitudes and population densities for the period 1951-99. We generated projections from six mosquito-borne disease models, driven by four global circulation models, using four representative concentration pathways, and three shared socioeconomic pathways. FINDINGS: We show that malaria suitability will increase by 1·6 additional months (mean 0·5, SE 0·03) in tropical highlands in the African region, the Eastern Mediterranean region, and the region of the Americas. Dengue suitability will increase in lowlands in the Western Pacific region and the Eastern Mediterranean region by 4·0 additional months (mean 1·7, SE 0·2). Increases in the climatic suitability of both diseases will be greater in rural areas than in urban areas. The epidemic belt for both diseases will expand towards temperate areas. The population at risk of both diseases might increase by up to 4·7 additional billion people by 2070 relative to 1970-99, particularly in lowlands and urban areas. INTERPRETATION: Rising global mean temperature will increase the climatic suitability of both diseases particularly in already endemic areas. The predicted expansion towards higher altitudes and temperate regions suggests that outbreaks can occur in areas where people might be immunologically naive and public health systems unprepared. The population at risk of malaria and dengue will be higher in densely populated urban areas in the WHO African region, South-East Asia region, and the region of the Americas, although we did not account for urban-heat island effects, which can further alter the risk of disease transmission. FUNDING: UK Space Agency, Royal Society, UK National Institute for Health Research, and Swedish Research Council.

Dynamical Malaria Forecasts Are Skillful at Regional and Local Scales in Uganda up to 4 Months Ahead.

Malaria forecasts from dynamical systems have never been attempted at the health district or local clinic catchment scale, and so their usefulness for public health preparedness and response at the local level is fundamentally unknown. A pilot preoperational forecasting system is introduced in which the European Centre for Medium Range Weather Forecasts ensemble prediction system and seasonal climate forecasts of temperature and rainfall are used to drive the uncalibrated dynamical malaria model VECTRI to predict anomalies in transmission intensity 4 months ahead. It is demonstrated that the system has statistically significant skill at a number of sentinel sites in Uganda with high-quality data. Skill is also found at approximately 50% of the Ugandan health districts despite inherent uncertainties of unconfirmed health reports. A cost-loss economic analysis at three example sentinel sites indicates that the forecast system can have a positive economic benefit across a broad range of intermediate cost-loss ratios and frequency of transmission anomalies. We argue that such an analysis is a necessary first step in the attempt to translate climate-driven malaria information to policy-relevant decisions.

Uncertainty in malaria simulations in the highlands of Kenya: Relative contributions of model parameter setting, driving climate and initial condition errors.

In this study, experiments are conducted to gauge the relative importance of model, initial condition, and driving climate uncertainty for simulations of malaria transmission at a highland plantation in Kericho, Kenya. A genetic algorithm calibrates each of these three factors within their assessed prior uncertainty in turn to see which allows the best fit to a timeseries of confirmed cases. It is shown that for high altitude locations close to the threshold for transmission, the spatial representativeness uncertainty for climate, in particular temperature, dominates the uncertainty due to model parameter settings. Initial condition uncertainty plays little role after the first two years, and is thus important in the early warning system context, but negligible for decadal and climate change investigations. Thus, while reducing uncertainty in the model parameters would improve the quality of the simulations, the uncertainty in the temperature driving data is critical. It is emphasized that this result is a function of the mean climate of the location itself, and it is shown that model uncertainty would be relatively more important at warmer, lower altitude locations.

Assessment of malaria transmission changes in Africa, due to the climate impact of land use change using Coupled Model Intercomparison Project Phase 5 earth system models.

Using mathematical modelling tools, we assessed the potential for land use change (LUC) associated with the Intergovernmental Panel on Climate Change low- and high-end emission scenarios (RCP2.6 and RCP8.5) to impact malaria transmission in Africa. To drive a spatially explicit, dynamical malaria model, data from the four available earth system models (ESMs) that contributed to the LUC experiment of the Fifth Climate Model Intercomparison Project are used. Despite the limited size of the ESM ensemble, stark differences in the assessment of how LUC can impact climate are revealed. In three out of four ESMs, the impact of LUC on precipitation and temperature over the next century is limited, resulting in no significant change in malaria transmission. However, in one ESM, LUC leads to increases in precipitation under scenario RCP2.6, and increases in temperature in areas of land use conversion to farmland under both scenarios. The result is a more intense transmission and longer transmission seasons in the southeast of the continent, most notably in Mozambique and southern Tanzania. In contrast, warming associated with LUC in the Sahel region reduces risk in this model, as temperatures are already above the 25-30°C threshold at which transmission peaks. The differences between the ESMs emphasise the uncertainty in such assessments. It is also recalled that the modelling framework is unable to adequately represent local-scale changes in climate due to LUC, which some field studies indicate could be significant.

Migration statistics relevant for malaria transmission in Senegal derived from mobile phone data and used in an agent-based migration model.

One year of mobile phone location data from Senegal is analysed to determine the characteristics of journeys that result in an overnight stay, and are thus relevant for malaria transmission. Defining the home location of each person as the place of most frequent calls, it is found that approximately 60% of people who spend nights away from home have regular destinations that are repeatedly visited, although only 10% have 3 or more regular destinations. The number of journeys involving overnight stays peaks at a distance of 50 km, although roughly half of such journeys exceed 100 km. Most visits only involve a stay of one or two nights away from home, with just 4% exceeding one week. A new agent-based migration model is introduced, based on a gravity model adapted to represent overnight journeys. Each agent makes journeys involving overnight stays to either regular or random locations, with journey and destination probabilities taken from the mobile phone dataset. Preliminary simulations show that the agent-based model can approximately reproduce the patterns of migration involving overnight stays.

To what extent does climate explain variations in reported malaria cases in early 20th century Uganda?

Malaria case statistics were analysed for the period 1926 to 1960 to identify inter-annual variations in malaria cases for the Uganda Protectorate. The analysis shows the mid-to-late 1930s to be a period of increased reported cases. After World War II, malaria cases trend down to a relative minimum in the early 1950s, before increasing rapidly after 1953 to the end of the decade. Data for the Western Province confirm these national trends, which at the time were attributed to a wide range of causes, including land development and management schemes, population mobility, interventions and misdiagnosis. Climate was occasionally proposed as a contributor to enhanced case numbers, and unusual precipitation patterns were held responsible; temperature was rarely, if ever, considered. In this study, a dynamical malaria model was driven with available precipitation and temperature data from the period for five stations located across a range of environments in Uganda. In line with the historical data, the simulations produced relatively enhanced transmission in the 1930s, although there is considerable variability between locations. In all locations, malaria transmission was low in the late 1940s and early 1950s, steeply increasing after 1954. Results indicate that past climate variability explains some of the variations in numbers of reported malaria cases. The impact of multiannual variability in temperature, while only on the order of 0.5°C, was sufficient to drive some of the trends observed in the statistics and thus the role of climate was likely underestimated in the contemporary reports. As the elimination campaigns of the 1960s followed this partly climate-driven increase in malaria, this emphasises the need to account for climate when planning and evaluating intervention strategies.

A breeding site model for regional, dynamical malaria simulations evaluated using in situ temporary ponds observations.

Daily observations of potential mosquito developmental habitats in a suburb of Kumasi in central Ghana reveal a strong variability in their water persistence times, which ranged between 11 and 81 days. The persistence of the ponds was strongly tied with rainfall, location and size of the puddles. A simple power-law relationship is found to fit the relationship between the average pond depth and area well. A prognostic water balance model is derived that describes the temporal evolution of the pond area and depth, incorporating the power-law geometrical relation. Pond area increases in response to rainfall, while evaporation and infiltration act as sink terms. Based on a range of evaluation metrics, the prognostic model is judged to provide a good representation of the pond coverage evolution at most sites. Finally, we demonstrate that the prognostic equation can be generalised and equally applied to a grid-cell to derive a fractional pond coverage, and thus can be implemented in spatially distributed models for relevant vector- borne diseases such as malaria.

Assessing the effects of air temperature and rainfall on malaria incidence: an epidemiological study across Rwanda and Uganda.

We investigate the short-term effects of air temperature, rainfall, and socioeconomic indicators on malaria incidence across Rwanda and Uganda from 2002 to 2011. Delayed and nonlinear effects of temperature and rainfall data are estimated using generalised additive mixed models with a distributed lag nonlinear specification. A time series cross-validation algorithm is implemented to select the best subset of socioeconomic predictors and to define the degree of smoothing of the weather variables. Our findings show that trends in malaria incidence agree well with variations in both temperature and rainfall in both countries, although factors other than climate seem to play an important role too. The estimated short-term effects of air temperature and precipitation are nonlinear, in agreement with previous research and the ecology of the disease. These effects are robust to the effects of temporal correlation. The effects of socioeconomic data are difficult to ascertain and require further evaluation with longer time series. Climate-informed models had lower error estimates compared to models with no climatic information in 77 and 60% of the districts in Rwanda and Uganda, respectively. Our results highlight the importance of using climatic information in the analysis of malaria surveillance data, and show potential for the development of climate informed malaria early warning systems.

Mosquito breeding site water temperature observations and simulations towards improved vector-borne disease models for Africa.

An energy budget model is developed to predict water temperature of typical mosquito larval developmental habitats. It assumes a homogeneous mixed water column driven by empirically derived fluxes. The model shows good agreement at both hourly and daily time scales with 10-min temporal resolution observed water temperatures, monitored between June and November 2013 within a peri-urban area of Kumasi, Ghana. There was a close match between larvae development times calculated using either the model-derived or observed water temperatures. The water temperature scheme represents a significant improvement over assuming the water temperature to be equal to air temperature. The energy budget model requires observed minimum and maximum temperatures, information that is generally available from weather stations. Our results show that hourly variations in water temperature are important for the simulation of aquatic-stage development times. By contrast, we found that larval development is insensitive to sub-hourly variations. Modelling suggests that in addition to water temperature, accurate estimation of degree-day development time is very important to correctly predict the larvae development times. The results highlight the potential of the model to predict water temperature of temporary bodies of surface water. Our study represents an important contribution towards the improvement of weatherdriven dynamical disease models, including those designed for malaria early forecasting systems.

Projecting malaria hazard from climate change in eastern Africa using large ensembles to estimate uncertainty.

The effect of climate change on the spatiotemporal dynamics of malaria transmission is studied using an unprecedented ensemble of climate projections, employing three diverse bias correction and downscaling techniques, in order to partially account for uncertainty in climate- driven malaria projections. These large climate ensembles drive two dynamical and spatially explicit epidemiological malaria models to provide future hazard projections for the focus region of eastern Africa. While the two malaria models produce very distinct transmission patterns for the recent climate, their response to future climate change is similar in terms of sign and spatial distribution, with malaria transmission moving to higher altitudes in the East African Community (EAC) region, while transmission reduces in lowland, marginal transmission zones such as South Sudan. The climate model ensemble generally projects warmer and wetter conditions over EAC. The simulated malaria response appears to be driven by temperature rather than precipitation effects. This reduces the uncertainty due to the climate models, as precipitation trends in tropical regions are very diverse, projecting both drier and wetter conditions with the current state-of-the-art climate model ensemble. The magnitude of the projected changes differed considerably between the two dynamical malaria models, with one much more sensitive to climate change, highlighting that uncertainty in the malaria projections is also associated with the disease modelling approach.