Climate Change and Vector-borne Diseases: Where Are We Next Heading?

(See the major article by Boyce et al on pages 1403–10.)

Vector-borne diseases (VBDs) are transmitted by arthropod insects such as mosquitoes, ticks, flies, midges, and fleas. They account for about 17% of the estimated burden of all infectious diseases affecting humans, and they also exert pressure on food security through their impacts on animal health and plants. The VBD causing the greatest impact on humans is malaria, with an estimated 438 000 related deaths worldwide in 2015 [1]. The malaria parasite is transmitted to humans by the bites of Anopheles mosquitoes. The tropical form of this parasite (Plasmodium falciparum) is the most harmful and has a significant impact on vulnerable people, such as children, pregnant women, immunocompromised individuals, and elderly people. This is especially true in Africa, where 90% of all malaria-related deaths were reported in 2015 [1].

Like most VBDs, malaria is a climate-sensitive disease. Rainfall creates suitable conditions for mosquito-breeding sites, and temperature conditions modulate the development, aggressiveness, and mortality of the vector while also impacting the incubation period of the Plasmodium parasite inside the mosquito vector. There is a suitable temperature window for malaria transmission; if the local climate is too cold (<18°C for P. falciparum), it takes too long for the parasite to develop within the mosquito vector, while if the local climate gets too warm (>37°C), mosquito survival decreases dramatically. This is why tropical highlands and desert areas are generally malaria free. As an example of climate effects on malaria, approximately 3 million people contracted malaria in 1958 over the Ethiopian highlands, owing to increased transmission caused by greater-than-normal rainfall and higher-than normal temperatures [2]. A recent climate change risk assessment based on a multimodel ensemble shows that future climatic suitability for malaria is simulated to increase over the tropical highland regions, while it should decrease over the western plains of Africa [3, 4].

Floods can also strongly influence the occurrence of malaria epidemics via impacts upon vector populations. This happened in 1997–1998, when a substantial El Niño climate event caused significant flooding over eastern Africa. Large numbers of malaria deaths were subsequently reported in the northeastern lowlands of Kenya [5] and in southwestern Uganda [6]. Conversely, there was a significant decrease in the malaria burden in the highlands of Tanzania [7], possibly due to the flushing of mosquito larvae from breeding sites. These differences in flooding impact suggest the importance of geographical setting (topography and distance to water bodies) in influencing local malaria burden.

In this issue of The Journal of Infectious Diseases, Boyce et al investigate the impact of severe flooding in May 2013 on the malaria burden in Kasese District, western Uganda. For the first time, detailed data sets of malaria diagnostic tests and malaria-related hospital admissions were compared before and after the flooding in multiple villages, using a differences-in-differences approach, a method that accounts for background changes that might affect the outcome of interest. The impact of variables such as elevation and distance of the village to rivers on malaria risk was examined. The results suggest an increase of approximately 30% in the risk of individuals having a positive malaria diagnostic test result if their village bordered a flood-affected river as compared to villages farther from rivers, with a larger relative impact on upstream versus downstream villages. They further highlight the critical role of local geography in modulating the impacts of flooding. The authors conclude that extreme precipitation events, which might become more frequent with climate change, will pose significant challenges to future malaria control programs.

While climate plays an important role influencing VBDs via impacts on vectors and disease transmission, other critical factors need to be taken into account when trying to control human malaria. As suggested by Boyce et al, extreme rainfall events can also cause damage or destruction of health infrastructure. In addition, the future of the malaria landscape is likely to be influenced by a wider range of factors, such as population immunity, population vulnerability, population migration, disease control measures in place, the development of cost-effective vaccines, socioeconomic development, and land use. The impact of nonclimate drivers on malaria is reflected by drops in the number of malaria cases and deaths of 12% and 48%, respectively, over the African continent since 2000 [1]. These are a result of massive funding efforts that have improved vector control measures and the development of rapid diagnostic tests, despite changes in climate. This is evidence of significant progress in the control of malaria in Africa over the past 20 years for a multitude of reasons, many of which should be applicable to other VBDs.

The downward trend for malaria is not necessarily reflected in recent changes in other VBDs, however. For example, the incidence of dengue has increased 30-fold over the last 50 years, the incidence of tick-borne diseases (Lyme disease, tick-borne encephalitis, and babesiosis) is on the rise in temperate regions, important disease vectors have been reported at higher altitudes in the tropics [8, 9], sporadic autochthonous transmission of dengue fever and chikungunya have been reported in Croatia and France recently, and autochthonous transmission of Zika virus has emerged over the southeastern United States this summer. Climate plays an important role in setting the background for disease transmission. Milder winters in temperate regions are now more permissive for various pests to establish, and changes in temperature seasonality favor longer vector activity [10]. Negating climate effects, globalization, including the increase in travel of goods, people, and animals, is the main driver spreading pathogens and vectors around the globe [11]. The spread of the Asian tiger mosquito Aedes albopictus, the competent vector of dengue virus, chikungunya virus, and Zika virus, is one of the best examples illustrating this [12]. The outbreak of chikungunya that affected 200 people in Ravenna province in Italy in 2007 was triggered by a single infected traveler coming from the Indian subcontinent [13].

Focusing on the future, many interconnected drivers of disease are increasing in such a way as to encourage disease spread. Increased human population and consequent increases in food production, increased levels of travel and trade, increases in drug and insecticide resistance, climate change, and land use will undoubtedly favor the emergence of human and animal VBD into new regions. Improving disease surveillance systems, increasing the anticipatory activity and resilience of public health and veterinary public health services worldwide, and encouraging clinicians and scientists to work together to share data, share resources, and undertake interdisciplinary research in a One Health approach will be key to addressing the emerging VBD health challenges to come.

Notes

Acknowledgments. C. C. acknowledges support by The Farr Institute for Health Informatics Research MRC (grant MR/M0501633/1).

Potential conflicts of interest. All authors: No reported conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

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