More arboviral disease outbreaks in continental Europe due to the warming climate?

This is the authors' abstract. We don't add key points for this paper.

Arboviral diseases are a global public health threat increasingly affecting Europe. The West Nile virus infections largely associated with Culex spp. mosquitoes for example occurred uncharacteristically early in 2018 and were particularly severe in Europe, with over 2000 human cases, almost seven times that of the previous years.1,2 In addition to this record-breaking outbreak, the threat of further autochthonous outbreaks is increasing as a result of more frequent importations of dengue and chikungunya via travellers into Europe during the past decade. Dengue and chikungunya are both transmitted by Aedes aegypti and Aedes albopictus mosquitoes, both of which have undergone widespread global expansion due to increased global trade and travel.3,4 The primary vector A. aegypti favours warm and humid climatic conditions present in tropical and subtropical regions and is less tolerant of cooler temperatures than A. albopictus, since it is unable to produce eggs that undergo winter diapause.8 At present its establishment is limited to the Caucasus region of Europe and outermost regions of the European Union, although given the climatic suitability in southern continental Europe the possibility of future expansion remains. Currently, A. albopictus is a more relevant vector in regards to dengue and chikungunya risk in Europe as it is well established in many Mediterranean countries due to its better adaption to temperate climates and ecological plasticity. Although A. albopictus eggs can undergo winter diapause and survive in European climates, viral survival rate over winter is poor. Additionally, while A. aegypti favours human blood meals and thus tends to be found in indoor human settlements, A. albopictus feeds on a wider range of hosts and is a less competent vector for arboviruses.6 Overall A. albopictus is a less efficient vector for dengue and chikungunya virus transmission, and hence sustained outbreaks at higher latitudes where only A. albopictus is present are less likely to occur. Nevertheless, locally transmitted dengue and chikungunya cases in continental Europe where A. albopictus is present continue to occur at a greater frequency (Figure 1).7 Until 2010, Europe had been free of autochthonous dengue transmission, except for the 1927/28 outbreak in Greece. The 1927/28 outbreak involved A. aegypti, which inexplicably disappeared from Europe in the 1950s. However, A. albopictus was later discovered in 1979 in Albania for the first time in Europe, followed by subsequent detections of A. albopictus in Western Europe as a result of travel and trade.8 The first reports of locally contracted dengue cases in recent times occurred in Croatia (18 cases) and France (2 cases) in 2010. Since then, sporadic outbreaks have occurred in France in 2013, 2014, 2015 and 2018 and, most recently, in Spain in 2018 (Figure 1). All outbreaks occurred between the months of August and November, presumably as a result of importation via viremic travellers from dengue endemic areas, such as Guadeloupe and French Polynesia, to these regions where A. albopictus is established.9 Aedes albopictus vectorial capacity trend in southern Europe. In black, the modelled average VC of Aedes albopictus from 1979-2018 is shown for the European regions that have experienced local autochthonous transmission of dengue or chikungunya since 2007. The locally estimated scatterplot smoothed (LOESS) trend is shown in blue. This includes all regions along the Mediterranean Coast in Southern continental Europe between Croatia, Italy, France and Spain. (A) The timeline of recent dengue cases is shown in the bar graph, labelled with case numbers per country. The 2012 Madeira and the 2009 and 2018 Réunion dengue outbreaks are not included given the climatic and ecological differences between these islands and continental Europe. (B) The timeline of recent chikungunya cases is shown in the bar graph, labelled with case numbers per country. Again, past chikungunya outbreaks in Réunion are not included. Aside from imported cases, chikungunya was not present in Europe until 2007, when a large outbreak of chikungunya in Italy affected approximately 330 confirmed and probable cases from July through September via local A. albopictus transmission.3 The outbreak was traced back to an individual who had been in Kerala, India, where chikungunya is endemic. A similar event occurred again between August and November 2017, also in Italy, with 270 confirmed and 219 probable cases. Neither outbreaks sustained local transmission beyond the summer, meaning the virus had not overwintered. Additional autochthonous chikungunya transmission has occurred sporadically in France in 2010, 2014 and 2017, with 2, 12 and 17 cases, respectively. These events occurred between July and October, with index cases arriving from chikungunya-endemic countries such as India and Cameroon. As an ectotherm species, it is reasonable to examine the ambient climatic conditions of these outbreaks. One hypothesis as to why the frequency of these outbreaks seems to be increasing is that climate changes in southern Europe have impacted the vectorial capacity (VC) of A. albopictus.5 VC estimates the daily rate of human cases in a fully susceptible population. It is thus a measure of the ability for a vector to spread disease among humans and is derived from the basic reproduction number (R0). Figure 1 shows VC of A. albopictus for dengue and chikungunya over time, using Climatic Research Unit (CRU TS v. 4.01) climate data from 1950 to 2016 and Representative Concentration Pathway 2.6 climate projections for 2017 and 2018. The model is fully described in Liu-Helmersson et al.5 and calculates VC based on average daily vector biting rate, the probability of vector to human transmission per bite and vice versa, the duration of the extrinsic incubation period and the vector mortality rate. The associations between these parameters and diurnal temperature range specific to A. albopictus and dengue or chikungunya transmission were determined by data derived from the published literature and modelled to a 0.5 by 0.5 degree resolution over time. The resulting monthly rasters were subsequently averaged for each year and cropped over the southern continental Europe region, spanning along the Mediterranean from Croatia to Spain where past dengue and chikungunya infections have occurred from 2007 to 2018. Based on this model, VC for both dengue and chikungunya has been increasing since the introduction of A. albopictus in 1979 (Figure 1). This trend, if considered alongside the increase in returning travellers from dengue-endemic countries, may provide an interesting explanation for these outbreaks that warrants further research.10 Further analyses incorporating A. albopictus abundance estimates will be beneficial. The growing trend of travellers entering Europe from dengue or chikungunya-endemic countries raises the likelihood that these diseases will be imported and further spread by A. albopictus. Data from the International Air Travel Association (IATA) available from 2010 to 2017 indicate that the number of airplane passengers from these countries has increased considerably.11 Incoming IATA air passenger volume data for France, Spain and Croatia show there were approximately 7 700 000 passengers in 2010 from countries with dengue, which includes 112 countries based on estimates from the Institute for Health Metrics and Evaluation. This number grew to over 12 200 000 passengers in 2017 from 114 countries, representing an increase of almost 60%. Furthermore, data from the International Civil Aviation Organization show that total passenger volume in France, Spain and Croatia has been increasing steadily since the 1970s. Together these trends support increased travel as an explanation for the recent dengue outbreaks, although an examination of trends from chikungunya-endemic countries in addition to a more sophisticated analysis would be beneficial. For example, recent research has used IATA air passenger volume data to further target cities in Europe that receive large volumes of travellers from dengue-infected areas, such as Milan, Rome and Barcelona.10 Overall, spontaneous outbreaks of dengue and chikungunya are not unexpected due to the establishment of A. albopictus in Europe and the large volume of travellers arriving from endemic regions.8,10 Currently, the risk of sustained outbreaks is low.12 However, this trend of VC alongside the timeline of autochthonous outbreaks is intriguing and might be a contributing factor to increasing the vector competency and distribution of A. albopictus. This includes dispersal along highway networks and waterways, viral adaptations to A. albopictus and further increases in VC with climate changes. In addition, future climate changes may result in milder winters that allow for viral overwintering in eggs and thus sustained outbreaks. Conflict of interest: None declared.