Climate change and pestilence: vector-borne diseases in a changing world

Vector-borne diseases matter

Vector-borne diseases (VBDs) are infectious diseases often caused by the bite of an arthropod vector to a human, animal or plant host. Examples include the transmission of malaria protozoans or dengue viruses by mosquitoes, the transmission of plague bacteria Yersinia pestis by fleas or the transmission of the bacterium Xylella fastidiosa by xylem-feeding insects to plants, such as our precious and ancient olive trees.

“They were given power over a fourth of the earth to kill by sword, famine, plague, and by the wild beasts of the earth”, Revelation 6:8.

VBDs have always played a major role in history. In the Bible, “bugs” affecting humans and “pestilence” affecting livestock are two of the Egyptian plagues, and the fourth Horseman of the Apocalypse, pestilence, impersonates infectious diseases and illnesses. During the 14th century, the Black Death almost wiped out between a third and a half of the European population, and more recently, a large Zika virus outbreak, transmitted by the bite of infected Aedes mosquitoes, greatly affected Latin America and shook the world in 2015–16. Diseases with exotic names such as West Nile fever, chikungunya and dengue fever are nowadays transmitted in temperate regions of Europe, Asia and North America.

Surprise, climate is changing and is impacting all species on the planet

The climate is changing; and such rapid change has no analog over the past millennium [1]. Our emissions of greenhouse gases are responsible for these rapid and drastic changes; we are now living in the Anthropocene [2]. One of us remembers endless arguments between scientists and global warming sceptics during the early 2000s, now it’s evident, we just wasted precious time. Climate scientists were correct, and we are observing the first impacts of climate change before heading into turbulent 2020s. We are so to speak savoring the starters; sadly, the main course and the cheese board are still on the menu. Our children and grandchildren will have to pay the whole restaurant bill if we do not act rapidly. The younger generation seems to realize how important the climate change issue is and how expensive this bill will be; hence children have already started striking for their future.

When climate and temperature change, it obviously impacts all species on board, Homo sapiens included; and it can cause all sorts of expected and unexpected chain reactions. From big polar bears that move southward to find food, to tiny insects and the diseases they potentially bring with them that move northward as temperature conditions are getting more suitable. The temperature impacts the vector’s development, its mortality and biting rate. Moreover, at higher temperatures, the pathogen inside the arthropod’s body also replicates faster, so that the vector can transmit it faster. These epidemiological parameters can be combined into the maximum daily reproductive rate of the disease: the vectorial capacity which is derived from the Ross-MacDonald mathematical model framework [3].

The relationship between vectorial capacity and temperature depends on the particular pathogen and vector under study. Some vectors, and the pathogens they can transmit, are adapted to temperate environments while others are adapted to tropical or semi-tropical climates. As the climate changes, some regions might become suitable for a particular disease to occur; while others might become too warm, depending on the shape of this curve and local climatic conditions. Some regions might also become too dry, a lack of rainfall will leave mosquitoes without suitable breeding sites. Along with distribution change, transmission seasons might lengthen or shorten as well. It is noteworthy that rapid climatic change might have favored the plagues of Egypt too [6].

“The increase in atmospheric greenhouse gases concentration will enhance the greenhouse effect, resulting on average in an additional warming of the Earth’s surface”, IPCC-AR1 report, 1992.

Recent trends – a storm of different factors

The environment sets the background for a particular species to flourish or perish in a given location, depending on its ecological plasticity and capacity to adapt. However, humans, and other migratory species like birds, are introducing vectors and pathogens into new regions. Rattus norvegicus, the common brown rat, spread worldwide in English ships and carried fleas infected with Y. pestis. More recently, the Asian tiger mosquito Ae. albopictus, was introduced into Europe, North America and Africa by the shipment of goods, primarily in used tires and plants [7]. Ae. albopictus can transmit chikungunya, dengue and Zika virus to humans and filarial nematodes to dogs. We were both involved with interdisciplinary teams involving scientists at the University of Liverpool and Public Health England (PHE; both UK) that investigated how recent and future climate conditions could become suitable for this mosquito using different mathematical models [8,9]. We found that 1) recent climate conditions were already suitable for Ae. albopictus to establish itself over a large part of Europe, and that 2) future climate change might expand its range farther north and east in future. Notably, southern UK was simulated to be suitable for this mosquito species in future.

Sadly, our simulations anticipated the observed spread of the Asian tiger mosquito into Europe and even into the UK [10,11]. Colleagues at PHE found Ae. albopictus eggs and larvae in Kent, southern UK, in 2016, 2017 and 2018 (though no adults were found to date) [10]. This is important because local transmission of dengue, which was constrained to the tropics 20 years ago, can now be observed in southern France or Barcelona [12]. In these cases, infected travelers are returning from tropical countries and introduce the pathogens into vector endemic regions. Here, minor disease transmission is now possible during and following the warmest summer months.

Other scientific teams found similar results using different methods. Increased risks posed by ticks, soil helminths and other insect vectors in temperate and peri-arctic regions were anticipated by several teams worldwide [13]. An increased mobility and rapid changes in environmental conditions are thought to be responsible for these changes in vector and VBD distributions. In addition, insecticide and drug resistance are on the rise too, posing an additional threat to current and future health. Fortunately, modern medicine and public health services are shielding us against such diseases – when such services exist. Socio-economic development is usually the key factor in modulating the burden of VBDs in a given country.

To conclude

“You do not respond to a mosquito bite with a hammer.” PLO Lumumba

Rapid environmental and climate changes, coupled with increased mobility of goods and persons, will undoubtedly impact the distribution of VBDs in future. It is noteworthy that such VBDs were already plaguing us in the past, and the development of modern medicine, public health and vector control measures significantly improved the situation at global scale. The scientific community anticipated important climate change impacts, almost 20 years ago. Given the recent geo-political climate, a seemingly increasing mistrust in science (anti-vaxers, flat earthers…) and the increase in drug and insecticide resistance, the upcoming 20 years are going to be extremely challenging.

One of the standard questions we often get asked is ‘Why do mosquitoes exist?’. From an external observer point of view, they act as a source of food for amphibians, fish, birds, reptiles and other insects, though it is debatable if the ecosystems would not just be the same without them [14]. From the mosquito point of view, it’s a matter of survival: females need blood to lay eggs. From Homo sapiens point of view, they’re seen as biting nuisance and potential source of diseases, hence our need to use vector control methods in order to improve human, animal and plant health.