Climate change and the spread of Aedes mosquito-borne viruses in Europe

ABSTRACT

Several outbreaks of chikungunya and dengue occurred on Mediterranean coasts during the hot season in the last two decades. Aedes albopictus was the vector involved in all the events. As a consequence of climate change, the ‘Tiger’ mosquito is now spreading through central Europe, and in the summer of 2023, for the first time, mosquito control measures were implemented in Paris to prevent autochthonous transmission of dengue. Rapid changes in the distribution of tropical disease vectors need to be taken into account in future risk assessment activities.

On August 31, health authorities recommended, for the first time, fumigation of some areas of Paris, and insecticide was sprayed on trees, green spaces, and other potential mosquito-breeding grounds, for 150 m around the home of persons who had acquired dengue while traveling in endemic countries (https://www.lemonde.fr<2023/08/31). This measure was implemented because Aedes albopictus (the Asian ‘Tiger’ mosquito), after establishing in Mediterranean Europe, is now rapidly advancing through Central and Northern Europe as a consequence of climate change [1]. Thus, autochthonous transmission of dengue and other tropical vectorborne viruses, already reported in Southern Europe, is becoming a concrete risk also for previously unaffected areas, such as the Île of France.

Actually, dengue epidemics were not uncommon in the Mediterranean basin at the beginning of the last century, and a major outbreak occurred in Athens in 1927–1928. However, the vector of the dengue virus at that time was Aedes aegypti (whose eggs are less resistant to low temperature than those of Ae. Albopictus), which disappeared after 1935 [2]. Shortly after that major epidemic, Dengue abandoned Europe for a long time, and Aedes mosquito-borne virus outbreaks were not identified up to the first decade of this century.

At the end of August 2007, an outbreak of chikungunya (>300 cases), another Aedes mosquito-borne disease, occurred in two small Italian villages [3]. The outbreak started after a viremic person coming from Kerala, India, visited his relatives living in one of the villages, which were heavily infested by Ae. albopictus mosquitoes. The outbreak revealed the vulnerability of temperate climate countries in the era of globalization and rapid transportation. Ten years later, in 2017, another major chikungunya outbreak (almost 500 cases) was identified in Italy [4]. Meanwhile, local clusters and small outbreaks of chikungunya occurred also in France, where 2 cases were identified in 2010, 12 in 2014, and 17 in 2017 [5,6].

Dengue reappeared on North-Mediterranean coasts in the summer of 2010, when two cases of local transmission were reported in Southern France, followed by a single case in 2013 [7]. On mid-August of the year 2010, an outbreak of dengue occurred in Croatia, approximately 100 km north-west of Dubrovnik, where dengue-specific antibodies were found in more than 5% of the serum samples collected on October 2010 [8]. Thereafter, a series of local transmission events occurred on the Mediterranean coasts of three European countries (France, Italy, and Spain). Autochthonous transmission of dengue continued to be reported at increasing levels in the last couple of years, with 71 cases (65 cases belonging to 9 different clusters in France and 6 in Spain) identified in 2022, and at least 72 cases (belonging to 3 different clusters in Italy and 41 (7 clusters) in France plus 3 cases in Spain, in 2023 [7]).

In all the epidemic events occurred in Europe, virus transmission was sustained by Ae. albopictus, which is conquering new lands, becoming extremely important in the spread of tropical infectious diseases in temperate climate areas, while Aedes aegypti, which has recently established in Cyprus (https://ecdc.europa.eu/en/disease-vectors/surveillance-and-disease-data/mosquito-maps), remains the main competent vector of chikungunya and dengue virus transmission worldwide [9].

Aedes albopictus reached Southern Europe more than 30 years ago. Italy was the first European country where the presence of the ‘tiger’ mosquito was recognized, in the early 90s, well before the occurrence of the first chikungunya outbreak. This mosquito was introduced through the shipment of secondhand tires infested with their eggs, and then spread through the Country, demonstrating a high capacity to breed in a huge variety of disposable containers and ground water collection sites [9–11]. Thereafter, the Asian Tiger mosquito established on the Mediterranean coasts of all the other European countries.

So far, the main determinant of outbreaks transmitted by Ae. albopictus in Europe has been represented by the dual globalization of humans and mosquitoes, and local transmissione has occurred exclusively in ‘part-time’ tropical countries of Southern Europe during the hot season, being limited in time and space. Changes in temperature and in the pattern of humidity and precipitation, along with the urban ‘heat island effect’, might now fuel the reproduction and spread of mosquito populations, influencing the activity of vectorborne viral infections in different ways [1,12,13]. Thus, the main question is to what extent climate change will favor the establishment and the activity of Aedes spp. mosquitoes (not only Ae. albopictus but also Ae. aegypti and eventually the newly detected Ae. Koreicus) even beyond the Mediterranean area, influencing mosquito-borne virus dynamics in Europe [14].

Major changes in the climate could have two different types of consequences. Firstly, in Mediterranean Europe, the hot season might be prolonged, favoring a more intense and durable activity of Ae. mosquitoes; this could result in larger-scale epidemics of dengue and/or chikungunya and in virus overwintering due to continued human-mosquito-human transmission – though at low level – during the winter, which could lead to an endemic state. In fact, vertical transmission of dengue and chikungunya viruses from adult mosquitoes to their offspring (also defined as ‘transovarial transmission’) is not very efficient, thus prolonged mosquito activity is needed to allow viruses to overcome the cold season. Secondly, climate change is favoring the establishment of Aedes mosquitoes in cooler areas of Central and Northern Europe, which have not been affected so far. What happened in Paris is a clear signal of this trend and urges for an update of vectorborne viruses risk assessment.

Funding Statement

The author(s) reported that there is no funding associated with the work featured in this article.

Disclosure statement

No potential conflict of interest was reported by the author.