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Climate change: an enduring challenge for


vector-borne disease prevention and control
Climate change is already affecting vector-borne disease transmission and spread, and its impacts are likely to
worsen. In the face of ongoing climate change, we must intensify efforts to prevent and control vector-borne diseases.

Joacim Rocklöv and Robert Dubrow

T
he rapid warming of the Earth, caused cycle; while there has been an increase in non-human hosts (Table 1). For example,
by anthropogenic greenhouse gas overall global precipitation, some areas have for Lyme disease, small mammals and
emissions, has profound long-term become wetter and others have become birds serve as competent (reservoir) hosts
implications for the prevention and control drier. Both wet and dry regions, however, (they are infected by the tick vector and
of vector-borne diseases. Put simply, vectors, have experienced an increase in extreme they can infect ticks); deer and other
which are ectotherms (that is, cold-blooded precipitation events. large- and medium-sized mammals serve
animals), do better in a warmer world. If current greenhouse gas emission trends as incompetent hosts (they provide adult
Here, we discuss how climate affects the continue, the mean global temperature could ticks with blood meals but do not become
transmission dynamics and geographic increase by 4 to 5 °C above preindustrial infected); and humans serve as dead-end
spread of vector-borne diseases and the levels by the end of the century2,3, which hosts (they are infected by ticks but do not
impact our changing climate has had thus would result in dramatic intensification of infect ticks). For West Nile virus, a wide
far. We emphasize how the presence of the changes already observed. According to range of bird species serve as reservoir
many non-climate drivers of vector-borne the authoritative Intergovernmental Panel hosts with a range of competence, whereas
disease transmission makes it difficult on Climate Change (IPCC), “Continued humans, horses and other mammals serve as
to isolate the role of climate change. We emission of greenhouse gases will cause dead-end hosts.
highlight the symbiotic intersection of further warming and long-lasting changes Among vector-borne diseases, malaria
(1) observational studies that elucidate how in all components of the climate system, is the major killer, causing an estimated
meteorological variables affect the incidence, increasing the likelihood of severe, pervasive 620,000 deaths in 2017 (most occurring
transmission-season duration and spread of and irreversible impacts for people and in Africa), followed by dengue, with an
vector-borne diseases and (2) scenario-based ecosystems”3. The impact of climate change estimated 40,500 deaths (most occurring in
modeling of the effects of future climate on the incidence, transmission season Asia)6. The estimated number of incident
change that can aid long-term planning for duration and spread of vector-borne diseases cases in 2017 was 209 million for malaria
the prevention and control of vector-borne represents a major threat4. and 105 million for dengue7. While most
diseases. Finally, to address the adverse other vector-borne neglected tropical
impacts of climate change, we call for urgent Vector-borne diseases diseases are seldom fatal, they involve
and rapid reductions in greenhouse gas A vector is an organism (most often an chronic infections that confer substantial
emissions, as well as adaptation to ongoing arthropod) that transmits an infectious disability. In 2017, an estimated 65 million
climate change through intensification of pathogen from an infected human or people were living with lymphatic filariasis,
vector-borne disease prevention and animal host to an uninfected human. The 143 million with schistosomiasis, 21 million
control efforts. World Health Organization identifies with onchocerciasis, 6.2 million with Chagas
the major global vector-borne diseases disease and 4.1 million with leishmaniasis7.
Climate change as malaria, dengue, chikungunya, yellow
Anthropogenic greenhouse gas emissions fever, Zika virus disease, lymphatic How climate affects vector-borne
have caused the mean global temperature filariasis, schistosomiasis, onchocerciasis, diseases
to increase by 1 °C above preindustrial Chagas disease, leishmaniasis and Japanese Climate can affect the transmission
levels1,2. The impacts of a 1 °C rise have encephalitis (Table 1)5. Other vector-borne dynamics, geographic spread and
been profound, including a decrease in diseases of regional importance include re-emergence of vector-borne diseases
the number of cold days and nights, an African trypanosomiasis, Lyme disease, through multiple pathways, including
increase in the number of warm days and tick-borne encephalitis and West Nile direct effects on the pathogen, the vector,
nights, an increase in extreme heat events, fever. Tropical and subtropical low- and non-human hosts and humans. In addition
decreased snow cover, and accelerating sea middle-income countries bear the highest to having direct effects on individual species,
level rise. Global warming has exhibited burden of vector-borne diseases. Eight climate change can alter entire ecosystem
considerable heterogeneity, with greater vector-borne diseases are considered to be habitats (including urban habitats), in which
warming over land than over the oceans, neglected tropical diseases (Table 1). vectors or non-human hosts may thrive
the greatest warming occurring in the Humans serve as the primary host for or fail.
Arctic, and evidence for greater warming some vector-borne diseases, including Because arthropods and other vectors
in winter versus summer and in nighttime malaria, dengue, chikungunya and Zika are ectotherms, it is expected that vector
versus daytime. Increased evaporation virus disease, whereas other vector-borne abundance, survival and feeding activity
from warming has resulted in complex, diseases have more complex transmission will increase with increasing temperature, as
region-specific changes in the hydrological dynamics, with both human and will the rate of development of the pathogen
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that the transmission season will lengthen in control measures. Thus, a suitable climate
some endemic areas. (Aedes albopictus, the is necessary but often not sufficient, as the
other dengue vector, has already exhibited climate determines the potential geographic
widespread expansion into more temperate distribution of a vector-borne disease,
regions; however, the role of climate change but other factors determine the actual
is unclear.) There is also the possibility of a distribution within the boundaries set
decrease in the incidence of dengue or other by climate.
vector-borne diseases in endemic areas if Non-climate drivers can be categorized
they become so hot that vector survival or into four groups: globalization and
feeding are inhibited. Such areas, however, environment, sociodemographics, public
would still face other severe impacts from health systems, and vector and pathogen
extreme heat. characteristics11 (Table 2). Despite climate
The relationship between precipitation change, during the past decade, substantial
and vector abundance is complex and progress has been made against many
context specific9. Increased precipitation vector-borne diseases. This progress has
could provide more vector breeding sites; been attributed to sociodemographic (for
however, drought could also provide more example, economic development) and public
breeding sites due to an increase in the health system (for example, vector control
use of containers for rainwater collection and other public health interventions)
and storage — prime breeding sites for A. drivers5. Between 2007 and 2017, the
aegypti. Vector abundance could also be age-standardized disability-adjusted life year
influenced by ecosystem change (for which (DALY) rates decreased by 39% for malaria,
climate change is a driver), which could 21% for yellow fever, 45% for lymphatic
degrade or enhance vector habitats and filariasis, 29% for schistosomiasis, 8% for
species competition, or it could increase or onchocerciasis, 23% for Chagas disease,
Credit: Chris Sharp reduce the abundance of vector predators or 56% for leishmaniasis and 83% for African
vector pathogens. trypanosomiasis12.
Abundance and behaviors of both Thus, economic development and
non-human and human hosts may be public health interventions —and not
within the vector. Thus, the extrinsic influenced by climate. Climate can influence climate change — appear to have been the
incubation period (the time between a non-human host directly, or it can do primary drivers of the incidence of these
ingestion of the pathogen by the vector so indirectly through ecosystem change, vector-borne diseases globally over the past
and the vector becoming infective) for the which can affect the abundance of food decade. It is possible that progress would
dengue virus has been found to be inversely sources, predators and pathogens, making have been even greater in the absence of
associated with ambient temperature8. In habitats either more or less hospitable. climate change, but this would be difficult
fact, an infected vector may never become For example, birds serve as the reservoir to convincingly demonstrate. Vector-borne
competent (capable of transmitting host for West Nile virus. The shift in bird disease drivers, including climate change,
infection) if the rate of development of migration patterns and decline in bird can affect and interact with each other, and
the pathogen is so slow or survival of the populations in North America, caused by the effect of one driver may be mediated
vector is so short that the vector dies before several factors — including climate change10 through processes linked to other drivers,
becoming infective. — may affect transmission of the virus making it difficult to isolate driver effects
Although ‘warmer is better’ for vectors in from Culex mosquitoes to humans. Human and thus to unambiguously attribute
general, relationships between temperature population displacement caused by climate changes in transmission or spread to
and vector survival, abundance and feeding change can spread the vector or pathogen to climate change. An additional problem in
behavior are often complex. For example, in new locations or can put immunologically disentangling climate change from other
the laboratory, survival of the dengue vector susceptible populations in contact with the effects is a lack of high-quality global-scale
Aedes aegypti from egg to adult increases vector and pathogen. observational data on disease incidence and
roughly linearly from near 0% at 15 °C to non-climate drivers.
about 90% at 20 °C and then slowly falls to Climate change and vector-borne Dengue is the only major global
about 60% at 35 °C; the time of development diseases vector-borne disease for which the
from egg to adult drops sharply from about There is no doubt that a suitable climate is age-standardized DALY rate increased
60 days at 15 °C to 12 days at 20 °C and then necessary for the persistence or emergence between 2007 and 2017, and it increased by
declines further to about 6 days at 27–34 °C; of a vector-borne disease. Thus, although 26%12. This trend represents a continuation
and the percentage of mosquitoes that travel-acquired cases of dengue occur in of the explosive expansion of dengue
complete a blood meal within 30 minutes Sweden, dengue is not endemic to Sweden since the 1950s, driven by urbanization,
after a host is made available plateaus at because neither the Aedes mosquito nor the globalization and ineffective mosquito
about 50% between 22 °C and 28 °C and virus are established there, due to unsuitable control13. Although climate has set
then declines to almost 0% at 33 °C (ref. 9). climatic conditions. However, there also are geographic limits on dengue expansion,
Clearly, the geographic range of A. many non-climate drivers that determine it would be difficult to demonstrate that
aegypti (and other vectors) is limited by whether a vector-borne disease is found climate change has been a contributing
cooler ambient temperatures. As the Earth in a particular geographic area (Table 2). factor on a global scale.
warms, the concerns are that the mosquito For example, malaria was present in the In summary, climate represents a critical
and virus will spread to higher latitudes and southern United States until the 1940s, factor in determining vector-borne disease
altitudes, that incidence will increase, and when it was eradicated by aggressive vector incidence, but it does not appear that climate

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Table 1 | Major global and regional vector-borne diseases


Disease Pathogen Primary vector(s) Primary non-human reservoir
(competent) hosts
Malaria Plasmodium parasite Anopheles mosquito Non-human hosts of minor concern
Dengue* Flavivirus Aedes aegypti and Aedes albopictus Non-human hosts of minor concern
mosquitoes
Yellow fever Flavivirus A. aegypti and A. albopictus mosquitoes Non-human primates
Zika Flavivirus A. aegypti and A. albopictus mosquitoes Non-human hosts of minor concern
Chikungunya* Alphavirus A. aegypti and A. albopictus mosquitoes Non-human hosts of minor concern
Lymphatic filariasis* Various filarial nematodes A variety of mosquito genera Non-human hosts of minor concern
Schistosomiasis* Schistosoma trematode Snail Non-human hosts of minor concern
Onchocerciasis* Onchocerca volvulus nematode Simulium (black fly) None
Chagas disease* Trypanosoma cruzi parasite Triatomine bug Mammals
Leishmaniasis* Leishmania parasite Sand fly Rodents, dogs, other mammals
Japanese encephalitis Flavivirus Culex mosquitoes Pigs, birds
African trypanosomiasis* Trypanosoma brucei parasite Glossina (tsetse fly) Wild and domestic animals
Lyme disease Borrelia spirochete Ixodes ticks White-footed mouse and other small
mammals, birds
Tick-borne encephalitis Flavivirus Ixodes ticks Small rodents
West Nile fever Flavivirus Culex mosquitoes Birds
Information sourced from the US Centers for Disease Control and Prevention and World Health Organization. *Considered by the World Health Organization to be neglected tropical diseases (https://www.who.
int/neglected_diseases/diseases/summary/en/).

change has been a primary driver thus far or is likely to affect vector-borne disease 2017 chikungunya outbreaks transmitted by
on a global scale. Nevertheless, there are transmission or spread. For example, a A. albopictus in Europe17 and the 2015–2016
serious reasons for concern. First, there have time-series analysis of monthly malaria Zika virus epidemic transmitted by A.
been numerous regional or local signals that cases in the highlands of Colombia and aegypti and A. albopictus in South America18.
climate change is affecting or will be likely Ethiopia provided evidence for a shift in the In the latter case, temperature conditions
to affect vector-borne disease incidence or altitudinal distribution of malaria toward associated with the 2015–2016 El Niño/
spread. Second, one would expect a time lag higher altitudes in warmer years, suggesting Southern Oscillation were exceptionally
between changes to the climate that make a that, in the absence of intervention, the conducive to Zika virus transmission.
non-endemic area suitable for endemicity, malaria burden will increase at higher Globally, vectorial capacity for both dengue
actual establishment of the vector and elevations as the climate warms14. vectors (A. aegypti and A. albopictus) has
pathogen in that area, and occurrence and Pathogens may be dispersed into been rising steadily since the 1980s, with
reporting of cases of disease. Third, climate non-endemic localities through travel, trade nine of the ten highest years occurring
change could emerge as a synergistic driver or migration. The number of dengue cases since 200019.
if there were backsliding on vector control imported into Europe is highly correlated In the United States, higher cumulative
measures and other public health efforts with the number of travelers arriving from growing degree days (a temperature metric),
due to complacency or a lack of political endemic zones15. Local (autochthonous) lower cumulative precipitation and lower
will. Fourth, one would expect pathogen outbreaks of dengue and chikungunya have saturation deficit (inversely related to
and vector evolution to accelerate in a occurred in southern Europe when infected humidity) were found to be associated
warming world due to higher replication travelers pass the pathogen to the mosquito with an earlier start to the Lyme disease
rates. Such evolution can play a significant vector A. albopictus (now established in season20. Higher temperature was found
role in vector-borne disease emergence, southern Europe), which in turn causes to be the most important determinant
re-emergence and spread (for example, secondary cases of human infection16. of environmental suitability for the
through pathogens evolving resistance to Although such outbreaks are still rare, and establishment of the Lyme disease Ixodes
treatment or vectors evolving resistance to the current risk of sustained outbreaks tick vector in southern Canada, where it has
pesticides). Finally, climate change will only is low, as the climate warms, vigilance is been spreading21. Milder and shorter winters
get worse in the foreseeable future, with needed to prevent sustained outbreaks or in Quebec, Canada are associated with the
models projecting a substantial expansion of establishment of endemicity in the future. northern spread of the white-footed mouse,
regions with a suitable climate for a number Vectorial capacity (a summary measure the primary reservoir host for the Lyme
of vector-borne diseases. of the capacity of a vector to transmit disease pathogen Borrelia burgdorferi22.
disease that integrates information on
Regional and local signals of climate vector abundance, survival, competence and Future climate change and
change effects on vector-borne diseases feeding rate, and the length of the extrinsic vector-borne diseases
There are many regional and local signals incubation period), which is dependent on Regional and local signals of the effect of
that climate change has already affected temperature conditions, helped explain the climate change on vector-borne diseases

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can be process-based (taking into account


Table 2 | Non-climate drivers of the transmission and spread of vector-borne diseases fundamental biological processes and
Globalization and environment mechanisms involved in transmission
dynamics) or empirical (based on
Driver Effect
observed statistical associations, without
Deforestation, mining and dams Change vector and non-human host habitats attempting to incorporate mechanisms).
Ecosystem degradation/change Changes vector and non-human host habitats Valid models depend on high-quality,
International travel and trade Spreads pathogen and vector
long-term observational data. Models are
disease-specific and are often valid for only a
Urbanization Provides an ideal habitat for A. aegypti specific geographic location or time period.
Population displacement Spreads pathogen to new locations or puts immunologically Due to difficulties in accurately
susceptible populations in contact with the vector and pathogen estimating mechanistic parameters,
Sociodemographic factors empirical models tend to be more feasible.
Driver Effect
Typically, these are time series models
that incorporate latency times between
Population demographic Children, the elderly and pregnant women may have elevated meteorological exposures and the disease
composition vulnerability outcome. For example, a study in Sri Lanka
Level of economic development Quality of housing (including presence of air conditioning) affects found dengue risk to be highest six to ten
exposure to vectors weeks following precipitation of more than
Baseline incidence of disease Vulnerability to climate change may be highest at the margins of 300 mm per week23. A study in Singapore
current endemic areas found that weekly mean temperature lagged
Population health status Low level of population health increases vulnerability by up to 16 weeks, weekly cumulative
precipitation lagged by up to 16 weeks,
Humanitarian crises War and famine confer high vulnerability
and season, trend of dengue cases and past
Public health systems dengue cases explained 84% of the variance
Driver Effect in dengue distribution24. Thus, past disease
Surveillance Passive and active surveillance inform prevention and control
incidence and other non-climate predictors
efforts (for example, population density) should be
evaluated for potential inclusion in models.
Early warning systems Preemptive vector control and other public health responses occur
Predicting how future climate change will
before impending outbreaks
affect vector-borne diseases is not possible
Vector control Vector control measures reduce vector abundance because there are too many uncertainties.
Quality of healthcare system Access to and quality of healthcare can affect size of infected First, how the climate will change will
human population, as well as case fatality rate and prevalence and depend on the aggressiveness of human
severity of disabilities actions to reduce greenhouse gas emissions.
Research Research on vector control, disease treatment, vaccine Second, prediction would need to take into
development, pathogen and vector evolution, and how to best account changes in non-climate drivers,
coordinate prevention and control efforts across sectors, can lead many of which are also unpredictable. For
to progress in control of vector-borne diseases example, how can we predict the pace of
Vector and pathogen characteristics development of more effective public health
interventions (for example, vector control
Driver Effect and vaccine development) or the political
Insecticide resistance Vector proliferation will needed for sustained efforts to control
Vector evolution Potential for greater vectorial capacity vector-borne diseases? Trends in these and
Pathogen drug resistance Increased pool of infected humans
other drivers are likely to be non-linear.
Although prediction is not possible,
Pathogen evolution Potential for higher pathogen transmissibility or virulence considerable effort has been devoted to
developing models based on alternative
scenarios to gain an understanding of a
indicate the need for vigilance. To address fact, greenhouse gas emissions continue to range of possible futures. Projections about
the vector-borne disease threat, along rise, and there is no evidence of worldwide the future incidence and distribution of a
with the many other severe risks posed political commitment to appreciably veer specific vector-borne disease are made by
by climate change, the world must meet from the current ‘business-as-usual’ path linking a future climate change scenario
the Paris Climate Agreement goal of that could lead to a 4–5 °C rise by 2100. (based on projected greenhouse gas
limiting global warming to no more than Prudence requires that we plan for a range of emissions) with a process-based or empirical
1.5 °C above preindustrial levels. This will possible futures. vector-borne disease model that has been
require immediate and steep reductions in First, we need to continue to validated using historical observational data.
greenhouse gas emissions through rapid and conduct observational studies, similar The simplest approach is to do this without
far-reaching changes in energy, land use, to the ones described in the previous incorporating scenarios for non-climate
transportation, urban, built environment, section, to understand the relationships drivers such as travel, socioeconomic factors
food and industrial systems1. between meteorological variables and or public health advances. This approach
However, our planet has already warmed vector-borne disease incidence and spread. asks: if the climate were to change according
by 1 °C, and limiting warming to another These studies usually involve applying to a particular scenario, but non-climate
0.5 °C is the absolute best we can do. In mathematical or statistical models, which drivers were to remain the same, what would

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be the effect on the vector-borne disease in RCP scenarios. The investigators found Health and Yale School of Medicine, Yale University,
question? Although simple, this approach that historical spread of these vectors, as New Haven, CT, USA. 3Yale Center on Climate
can help inform long-term planning, well as spread over the next 5–15 years, Change and Health, Yale University, New Haven,
according to the precautionary principle. could be explained by human movement CT, USA. 4These authors contributed equally:
The IPCC has developed four patterns, whereas in later years, expansion Joacim Rocklöv, Robert Dubrow.
Representative Concentration Pathway will be driven by climate change (especially ✉e-mail: robert.dubrow@yale.edu
(RCP) scenarios for greenhouse gas temperature increases) and urbanization,
emissions, ranging from a high-emission with higher emission scenarios associated Published online: 20 April 2020
‘business-as-usual’ scenario (RCP8.5) with greater expansion27. https://doi.org/10.1038/s41590-020-0648-y
to a low-emission, aggressive mitigation Thus, empirical models that incorporate
scenario (RCP2.6). For a given RCP, climate multiple predictors can help identify key References
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Acknowledgements
consistent decreases in tropical regions. modeling could help inform optimization J.R. received funding from the Swedish Research Council
The net effect of future climate change on of both current and future combinations of Formas (grant nos. 2018–01754 and 2017–01300) and the
future populations at risk was relatively interventions that will meet the enduring ZikaPlan project funded by the European Union research
small, although there were large regional challenges of prevention and control of and innovation program Horizon 2020 (grant agreement
differences. vector-borne diseases in the face of ongoing no. 734584). R.D. received funding from the High Tide
Foundation.
Another study used empirical global climate change. ❐
mosquito distribution data, meteorological Author contributions
variables and measures of urbanization Joacim Rocklöv1,4 and The authors worked collaboratively and contributed
and human mobility to build a model of Robert Dubrow   2,3,4 ✉ equally to the article.
historical spatial spread for A. aegypti 1
Department of Public Health and Clinical Medicine,
and A. albopictus, and used it to project Umeå University, Umeå, Sweden. 2Department of Competing interests
future spread until 2080 under different Environmental Health Sciences, Yale School of Public The authors declare no competing interests.

Nature Immunology | VOL 21 | May 2020 | 479–483 | www.nature.com/natureimmunology 483

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