El Niño and other climatic drivers of epidemic malaria in Ethiopia: new tools for national health adaptation plans.

BACKGROUND: Ethiopia has a history of climate related malaria epidemics. An improved understanding of malaria-climate interactions is needed to inform malaria control and national adaptation plans. METHODS: Malaria-climate associations in Ethiopia were assessed using (a) monthly climate data (1981-2016) from the Ethiopian National Meteorological Agency (NMA), (b) sea surface temperatures (SSTs) from the eastern Pacific, Indian Ocean and Tropical Atlantic and (c) historical malaria epidemic information obtained from the literature. Data analysed spanned 1950-2016. Individual analyses were undertaken over relevant time periods. The impact of the El Niño Southern Oscillation (ENSO) on seasonal and spatial patterns of rainfall and minimum temperature (Tmin) and maximum temperature (Tmax) was explored using NMA online Maprooms. The relationship of historic malaria epidemics (local or widespread) and concurrent ENSO phases (El Niño, Neutral, La Niña) and climate conditions (including drought) was explored in various ways. The relationships between SSTs (ENSO, Indian Ocean Dipole and Tropical Atlantic), rainfall, Tmin, Tmax and malaria epidemics in Amhara region were also explored. RESULTS: El Niño events are strongly related to higher Tmax across the country, drought in north-west Ethiopia during the July-August-September (JAS) rainy season and unusually heavy rain in the semi-arid south-east during the October-November-December (OND) season. La Niña conditions approximate the reverse. At the national level malaria epidemics mostly occur following the JAS rainy season and widespread epidemics are commonly associated with El Niño events when Tmax is high, and drought is common. In the Amhara region, malaria epidemics were not associated with ENSO, but with warm Tropical Atlantic SSTs and higher rainfall. CONCLUSION: Malaria-climate relationships in Ethiopia are complex, unravelling them requires good climate and malaria data (as well as data on potential confounders) and an understanding of the regional and local climate system. The development of climate informed early warning systems must, therefore, target a specific region and season when predictability is high and where the climate drivers of malaria are sufficiently well understood. An El Niño event is likely in the coming years. Warming temperatures, political instability in some regions, and declining investments from international donors, implies an increasing risk of climate-related malaria epidemics.

Climate-proofing a malaria eradication strategy.

Two recent initiatives, the World Health Organization (WHO) Strategic Advisory Group on Malaria Eradication and the Lancet Commission on Malaria Eradication, have assessed the feasibility of achieving global malaria eradication and proposed strategies to achieve it. Both reports rely on a climate-driven model of malaria transmission to conclude that long-term trends in climate will assist eradication efforts overall and, consequently, neither prioritize strategies to manage the effects of climate variability and change on malaria programming. This review discusses the pathways via which climate affects malaria and reviews the suitability of climate-driven models of malaria transmission to inform long-term strategies such as an eradication programme. Climate can influence malaria directly, through transmission dynamics, or indirectly, through myriad pathways including the many socioeconomic factors that underpin malaria risk. These indirect effects are largely unpredictable and so are not included in climate-driven disease models. Such models have been effective at predicting transmission from weeks to months ahead. However, due to several well-documented limitations, climate projections cannot accurately predict the medium- or long-term effects of climate change on malaria, especially on local scales. Long-term climate trends are shifting disease patterns, but climate shocks (extreme weather and climate events) and variability from sub-seasonal to decadal timeframes have a much greater influence than trends and are also more easily integrated into control programmes. In light of these conclusions, a pragmatic approach is proposed to assessing and managing the effects of climate variability and change on long-term malaria risk and on programmes to control, eliminate and ultimately eradicate the disease. A range of practical measures are proposed to climate-proof a malaria eradication strategy, which can be implemented today and will ensure that climate variability and change do not derail progress towards eradication.

Childhood malaria case incidence in Malawi between 2004 and 2017: spatio-temporal modelling of climate and non-climate factors.

BACKGROUND: Malaria transmission is influenced by a complex interplay of factors including climate, socio-economic, environmental factors and interventions. Malaria control efforts across Africa have shown a mixed impact. Climate driven factors may play an increasing role with climate change. Efforts to strengthen routine facility-based monthly malaria data collection across Africa create an increasingly valuable data source to interpret burden trends and monitor control programme progress. A better understanding of the association with other climatic and non-climatic drivers of malaria incidence over time and space may help guide and interpret the impact of interventions. METHODS: Routine monthly paediatric outpatient clinical malaria case data were compiled from 27 districts in Malawi between 2004 and 2017, and analysed in combination with data on climatic, environmental, socio-economic and interventional factors and district level population estimates. A spatio-temporal generalized linear mixed model was fitted using Bayesian inference, in order to quantify the strength of association of the various risk factors with district-level variation in clinical malaria rates in Malawi, and visualized using maps. RESULTS: Between 2004 and 2017 reported childhood clinical malaria case rates showed a slight increase, from 50 to 53 cases per 1000 population, with considerable variation across the country between climatic zones. Climatic and environmental factors, including average monthly air temperature and rainfall anomalies, normalized difference vegetative index (NDVI) and RDT use for diagnosis showed a significant relationship with malaria incidence. Temperature in the current month and in each of the 3 months prior showed a significant relationship with the disease incidence unlike rainfall anomaly which was associated with malaria incidence at only three months prior. Estimated risk maps show relatively high risk along the lake and Shire valley regions of Malawi. CONCLUSION: The modelling approach can identify locations likely to have unusually high or low risk of malaria incidence across Malawi, and distinguishes between contributions to risk that can be explained by measured risk-factors and unexplained residual spatial variation. Also, spatial statistical methods applied to readily available routine data provides an alternative information source that can supplement survey data in policy development and implementation to direct surveillance and intervention efforts.

Climate change and health: Moving from theory to practice.

In an Editorial discussing the Special Issue on Climate Change and Health, guest editors Jonathan Patz and Madeleine Thompson summarize key issues in the field and describe the significance of research studies included in the issue.

Prioritizing the needs of children in a changing climate.

In a Perspective, Lawrence Stanberry and colleagues discuss impacts of climate change on children.

Testing a multi-malaria-model ensemble against 30 years of data in the Kenyan highlands.

BACKGROUND: Multi-model ensembles could overcome challenges resulting from uncertainties in models' initial conditions, parameterization and structural imperfections. They could also quantify in a probabilistic way uncertainties in future climatic conditions and their impacts. METHODS: A four-malaria-model ensemble was implemented to assess the impact of long-term changes in climatic conditions on Plasmodium falciparum malaria morbidity observed in Kericho, in the highlands of Western Kenya, over the period 1979-2009. Input data included quality controlled temperature and rainfall records gathered at a nearby weather station over the historical periods 1979-2009 and 1980-2009, respectively. Simulations included models' sensitivities to changes in sets of parameters and analysis of non-linear changes in the mean duration of host's infectivity to vectors due to increased resistance to anti-malarial drugs. RESULTS: The ensemble explained from 32 to 38% of the variance of the observed P. falciparum malaria incidence. Obtained R²-values were above the results achieved with individual model simulation outputs. Up to 18.6% of the variance of malaria incidence could be attributed to the +0.19 to +0.25°C per decade significant long-term linear trend in near-surface air temperatures. On top of this 18.6%, at least 6% of the variance of malaria incidence could be related to the increased resistance to anti-malarial drugs. Ensemble simulations also suggest that climatic conditions have likely been less favourable to malaria transmission in Kericho in recent years. CONCLUSIONS: Long-term changes in climatic conditions and non-linear changes in the mean duration of host's infectivity are synergistically driving the increasing incidence of P. falciparum malaria in the Kenyan highlands. User-friendly, online-downloadable, open source mathematical tools, such as the one presented here, could improve decision-making processes of local and regional health authorities.

Effects of nitrogen fertilization and a commercial arbuscular mycorrhizal fungal inoculant on root rot and agronomic production of pea and lentil crops.

In the Canadian prairies, pulse crops such as field pea (Pisum sativum L.) and lentil (Lens culinaris L.) are economically important and widely grown. However, in recent years, root rot, caused by a variety of fungal and oomycete pathogens, including Aphanomyces euteiches, has become a limiting factor on yield. In this study, we examined the impacts of nitrogen (N) fertilization and a commercial arbuscular mycorrhizal fungal (AMF) inoculant on pea and lentil plant health and agronomic production at three locations in Saskatchewan: Swift Current, Indian Head and Melfort. The AMF inoculation had no impact on root rot severity, and therefore is not considered a reliable method to manage root rot in pea and lentil. In contrast, N fertilization led to reductions in root rot in Swift Current, but not the other two sites. However, N fertilization did reduce nodulation. When both pea and lentil are considered, the abundance of A. euteiches in soil increased from pre-seeding to mid-bloom. A negative correlation between soil pH and disease severity was also observed. The high between-site variability highlights the importance of testing root rot mitigation strategies under multiple soil conditions to develop site-specific recommendations. Use of N fertilizer as a root rot management strategy merits further exploration, including investigation into its interactions with other management strategies, soil properties, and costs and benefits.

The current landscape of software tools for the climate-sensitive infectious disease modelling community.

Climate-sensitive infectious disease modelling is crucial for public health planning and is underpinned by a complex network of software tools. We identified only 37 tools that incorporated both climate inputs and epidemiological information to produce an output of disease risk in one package, were transparently described and validated, were named (for future searching and versioning), and were accessible (ie, the code was published during the past 10 years or was available on a repository, web platform, or other user interface). We noted disproportionate representation of developers based at North American and European institutions. Most tools (n=30 [81%]) focused on vector-borne diseases, and more than half (n=16 [53%]) of these tools focused on malaria. Few tools (n=4 [11%]) focused on food-borne, respiratory, or water-borne diseases. The under-representation of tools for estimating outbreaks of directly transmitted diseases represents a major knowledge gap. Just over half (n=20 [54%]) of the tools assessed were described as operationalised, with many freely available online.

Raised temperatures over the Kericho tea estates: revisiting the climate in the East African highlands malaria debate.

BACKGROUND: Whether or not observed increases in malaria incidence in the Kenyan Highlands during the last thirty years are associated with co-varying changes in local temperature, possibly connected to global changes in climate, has been debated for over a decade. Studies, using differing data sets and methodologies, produced conflicting results regarding the occurrence of temperature trends and their likelihood of being responsible, at least in part, for the increases in malaria incidence in the highlands of western Kenya. A time series of quality controlled daily temperature and rainfall data from Kericho, in the Kenyan Highlands, may help resolve the controversy. If significant temperature trends over the last three decades have occurred then climate should be included (along with other factors such as land use change and drug resistance) as a potential driver of the observed increases in malaria in the region. METHODS: Over 30 years (1 January 1979 to 31 December 2009) of quality controlled daily observations ( > 97% complete) of maximum, minimum and mean temperature were used in the analysis of trends at Kericho meteorological station, sited in a tea growing area of Kenya's western highlands. Inhomogeneities in all the time series were identified and corrected. Linear trends were identified via a least-squares regression analysis with statistical significance assessed using a two-tailed t-test. These 'gold standard' meteorological observations were compared with spatially interpolated temperature datasets that have been developed for regional or global applications. The relationship of local climate processes with larger climate variations, including tropical sea surface temperatures (SST), and El Niño-Southern Oscillation (ENSO) was also assessed. RESULTS: An upward trend of ≈0.2°C/decade was observed in all three temperature variables (P < 0.01). Mean temperature variations in Kericho were associated with large-scale climate variations including tropical SST (r = 0.50; p < 0.01). Local rainfall was found to have inverse effects on minimum and maximum temperature. Three versions of a spatially interpolated temperature data set showed markedly different trends when compared with each other and with the Kericho station observations. CONCLUSION: This study presents evidence of a warming trend in observed maximum, minimum and mean temperatures at Kericho during the period 1979 to 2009 using gold standard meteorological observations. Although local factors may be contributing to these trends, the findings are consistent with variability and trends that have occurred in correlated global climate processes. Climate should therefore not be dismissed as a potential driver of observed increases in malaria seen in the region during recent decades, however its relative importance compared to other factors needs further elaboration. Climate services, pertinent to the achievement of development targets such as the Millennium Development Goals and the analysis of infectious disease in the context of climate variability and change are being developed and should increase the availability of relevant quality controlled climate data for improving development decisions. The malaria community should seize this opportunity to make their needs heard.

Effectiveness of malaria control during changing climate conditions in Eritrea, 1998-2003.

OBJECTIVE: To assess the effectiveness of impregnated mosquito nets, indoor residual spraying and larval control relative to the impacts of climate variability in the decline of malaria cases in Eritrea. METHODS: Monthly data on clinical malaria cases by subzoba (district) in three zobas (zones) of Eritrea for 1998-2003 were used in Poisson regression models to determine whether there is statistical evidence for reduction in cases by DDT, malathion, impregnated nets and larval control used over the period, while analysing the effects of satellite-derived climate variables in the same geographic areas. RESULTS: Both indoor residual spraying (with DDT or malathion) and impregnated nets were independently and significantly negatively associated with reduction in malaria cases, as was larval control in one zoba. Malaria cases were significantly positively related to differences in current and previous months' vegetation (NDVI) anomalies. The relationship to rainfall differences 2 and 3 months previously was also significant, but the direction of the effect varied by zoba. Standardized regression coefficients indicated a greater effect of climate in the zoba with less intense malaria transmission. CONCLUSION: The results support the view that both indoor residual spraying and impregnated nets have been independently effective against malaria, and that larval control was also effective in one area. Thus climate, while significant, is not the only explanation for the recent decline in malaria cases in Eritrea. If appropriate statistical approaches are used, routine surveillance data from cases attending health facilities can be useful for assessing control programme success and providing estimates of the effectiveness of individual control measures. Effectiveness estimates suitable for use in cost-effectiveness analysis have been obtained.

Improving the cost-effectiveness of IRS with climate informed health surveillance systems.

BACKGROUND: This paper examines how the cost-effectiveness of IRS varies depending on the severity of transmission and level of programme coverage and how efficiency could be improved by incorporating climate information into decision making for malaria control programmes as part of an integrated Malaria Early Warning and Response System (MEWS). METHODS: A climate driven model of malaria transmission was used to simulate cost-effectiveness of alternative IRS coverage levels over six epidemic and non-epidemic years. Decision rules for a potential MEWS system that triggers different IRS coverage are described. The average and marginal cost per case averted with baseline IRS coverage (24%) and under varying IRS coverage levels (50%, 75% and 100%) were calculated. RESULTS: Average cost-effectiveness of 24% coverage varies dramatically between years, from US$108 per case prevented in low transmission to US$0.42 in epidemic years. Similarly for higher coverage (24-100%) cost per case prevented is far higher in low than high transmission years ($108-$267 to $0.88-$2.26). DISCUSSION: Efficiency and health benefit gains could be achieved by implementing MEWS that provides timely, accurate information. Evidence from southern Africa, (especially Botswana) supports this. CONCLUSION: Advance knowledge of transmission severity can help managers make coverage decisions which optimise resource use and exploit efficiency gains if a fully integrated MEWS is in place alongside a health system with sufficient flexibility to modify control plans in response to information. More countries and programmes should be supported to use the best available evidence and science to integrate climate informed MEWS into decision making within malaria control programmes.

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.

Climate drivers of vector-borne diseases in Africa and their relevance to control programmes.

BACKGROUND: Climate-based disease forecasting has been proposed as a potential tool in climate change adaptation for the health sector. Here we explore the relevance of climate data, drivers and predictions for vector-borne disease control efforts in Africa. METHODS: Using data from a number of sources we explore rainfall and temperature across the African continent, from seasonality to variability at annual, multi-decadal and timescales consistent with climate change. We give particular attention to three regions defined as WHO-TDR study zones in Western, Eastern and Southern Africa. Our analyses include 1) time scale decomposition to establish the relative importance of year-to-year, decadal and long term trends in rainfall and temperature; 2) the impact of the El Niño Southern Oscillation (ENSO) on rainfall and temperature at the Pan African scale; 3) the impact of ENSO on the climate of Tanzania using high resolution climate products and 4) the potential predictability of the climate in different regions and seasons using Generalized Relative Operating Characteristics. We use these analyses to review the relevance of climate forecasts for applications in vector borne disease control across the continent. RESULTS: Timescale decomposition revealed long term warming in all three regions of Africa - at the level of 0.1-0.3 °C per decade. Decadal variations in rainfall were apparent in all regions and particularly pronounced in the Sahel and during the East African long rains (March-May). Year-to-year variability in both rainfall and temperature, in part associated with ENSO, were the dominant signal for climate variations on any timescale. Observed climate data and seasonal climate forecasts were identified as the most relevant sources of climate information for use in early warning systems for vector-borne diseases but the latter varied in skill by region and season. CONCLUSIONS: Adaptation to the vector-borne disease risks of climate variability and change is a priority for government and civil society in African countries. Understanding rainfall and temperature variations and trends at multiple timescales and their potential predictability is a necessary first step in the incorporation of relevant climate information into vector-borne disease control decision-making.

Data and tools to integrate climate and environmental information into public health.

BACKGROUND: During the last 30 years, the development of geographical information systems and satellites for Earth observation has made important progress in the monitoring of the weather, climate, environmental and anthropogenic factors that influence the reduction or the reemergence of vector-borne diseases. Analyses resulting from the combination of geographical information systems (GIS) and remote sensing have improved knowledge of climatic, environmental, and biodiversity factors influencing vector-borne diseases (VBDs) such as malaria, visceral leishmaniasis, dengue, Rift Valley fever, schistosomiasis, Chagas disease and leptospirosis. These knowledge and products developed using remotely sensed data helped and continue to help decision makers to better allocate limited resources in the fight against VBDs. MAIN BODY: Because VBDs are linked to climate and environment, we present here our experience during the last four years working with the projects under the, World Health Organization (WHO)/ The Special Programme for Research and Training in Tropical Diseases (TDR)-International Development Research Centre (IDRC) Research Initiative on VBDs and Climate Change to integrate climate and environmental information into research and decision-making processes. The following sections present the methodology we have developed, which uses remote sensing to monitor climate variability, environmental conditions, and their impacts on the dynamics of infectious diseases. We then show how remotely sensed data can be accessed and evaluated and how they can be integrated into research and decision-making processes for mapping risks, and creating Early Warning Systems, using two examples from the WHO TDR projects based on schistosomiasis analysis in South Africa and Trypanosomiasis in Tanzania. CONCLUSIONS: The tools presented in this article have been successfully used by the projects under the WHO/TDR-IDRC Research Initiative on VBDs and Climate Change. Combined with capacity building, they are an important piece of work which can significantly contribute to the goals of WHO Global Vector Control Response and to the Sustainable Development Goals especially those on health and climate action.

Malaria stratification, climate, and epidemic early warning in Eritrea.

Eritrea has a successful malaria control program, but it is still susceptible to devastating malaria epidemics. Monthly data on clinical malaria cases from 242 health facilities in 58 subzobas (districts) of Eritrea from 1996 to 2003 were used in a novel stratification process using principal component analysis and nonhierarchical clustering to define five areas with distinct malaria intensity and seasonality patterns, to guide future interventions and development of an epidemic early warning system. Relationships between monthly clinical malaria incidence by subzoba and monthly climate data from several sources, and with seasonal climate forecasts, were investigated. Remotely sensed climate data were averaged over the same subzoba geographic administrative units as the malaria cases. Although correlation was good between malaria anomalies and actual rainfall from ground stations (lagged by 2 months), the stations did not have sufficiently even coverage to be widely useful. Satellite derived rainfall from the Climate Prediction Center Merged Analysis of Precipitation was correlated with malaria incidence anomalies, with a lead time of 2-3 months. NDVI anomalies were highly correlated with malaria incidence anomalies, particularly in the semi-arid north of the country and along the northern Red Sea coast, which is a highly epidemic-prone area. Eritrea has 2 distinct rainy seasons in different parts of the country. The seasonal forecasting skill from Global Circulation Models for the June/July/August season was low except for the Eastern border. For the coastal October/November/December season, forecasting skill was good only during the 1997-1998 El Niño event. For epidemic control, shorter-range warning based on remotely sensed rainfall estimates and an enhanced epidemic early-detection system based on data derived for this study are needed.

Using Rainfall and Temperature Data in the Evaluation of National Malaria Control Programs in Africa.

Since 2010, the Roll Back Malaria (RBM) Partnership, including National Malaria Control Programs, donor agencies (e.g., President's Malaria Initiative and Global Fund), and other stakeholders have been evaluating the impact of scaling up malaria control interventions on all-cause under-five mortality in several countries in sub-Saharan Africa. The evaluation framework assesses whether the deployed interventions have had an impact on malaria morbidity and mortality and requires consideration of potential nonintervention influencers of transmission, such as drought/floods or higher temperatures. Herein, we assess the likely effect of climate on the assessment of the impact malaria interventions in 10 priority countries/regions in eastern, western, and southern Africa for the President's Malaria Initiative. We used newly available quality controlled Enhanced National Climate Services rainfall and temperature products as well as global climate products to investigate likely impacts of climate on malaria evaluations and test the assumption that changing the baseline period can significantly impact on the influence of climate in the assessment of interventions. Based on current baseline periods used in national malaria impact assessments, we identify three countries/regions where current evaluations may overestimate the impact of interventions (Tanzania, Zanzibar, Uganda) and three countries where current malaria evaluations may underestimate the impact of interventions (Mali, Senegal and Ethiopia). In four countries (Rwanda, Malawi, Mozambique, and Angola) there was no strong difference in climate suitability for malaria in the pre- and post-intervention period. In part, this may be due to data quality and analysis issues.