Vector-borne diseases are infections transmitted by the bite of infected arthropod species, such as mosquitoes, ticks, triatomine bugs, sandflies, and blackflies (1). Arthropod vectors are cold-blooded (ectothermic) and thus especially sensitive to climatic factors. Weather influences survival and reproduction rates of vectors (2), in turn influencing habitat suitability, distribution and abundance; intensity and temporal pattern of vector activity (particularly biting rates) throughout the year; and rates of development, survival and reproduction of pathogens within vectors. However, climate is only one of many factors influencing vector distribution, such as habitat destruction, land use, pesticide application, and host density. Vector-borne diseases are widespread in Europe and are the best studied diseases associated with climate change, which is reflected in this Review.
West Nile fever is caused by the West Nile virus, a virus of the family Flaviviridae which is part of the Japanese encephalitis antigenic group. West Nile fever mainly infects birds and infrequently human beings through the bite of an infected Culex mosquito.
In numerous European countries the virus has been isolated in mosquitoes, wild rodents, migrating birds, hard ticks, horses and human beings3. Since roughly 80% of cases are asymptomatic, the rate of West Nile virus infections in human beings remains largely unknown, and probably only some of the epidemics with tens or hundreds of West Nile fever cases have been documented4. Past entomologic data have been linked to meteorological data in order to model a West Nile fever outbreak in Southern France in 2000; the aggressiveness of the vector (Culex modestus) was positively correlated with temperature and humidity, and linked to rainfall and sunshine, which were particularly high during the epidemic period (5).
An outbreak in 1996-97 in southeastern Romania (6) resembled a subsequent outbreak in Israel in 2000, which was associated with a heat wave early in the summer with high minimum temperatures (7). These observations are in agreement with a climatic model for West Nile virus with mild winters, dry spring and summers, heat waves early in the season and wet autumns (8). Dry spells favour reproduction of city-dwelling mosquitoes (e.g. Culex pipiens) and concentrate vectors with their avian hosts around water sources, which leads to arbovirus multiplication (9). Explanatory models have assisted public-health practitioners in making decision about the spraying of preventative of preventive larvicides (10).
Dengue is the most important arboviral human disease, however, mainly due to nearly universal use of piped water the disease has disappeared from Europe (11). Dengue is frequently introduced into Europe by travelers returning from dengue-endemic countries but no local transmission has been reported since it would also depend on the reintroduction of its principal vector, the mosquito Aedes aegypti (yellow fever mosquito) which is adapted to urban environments. However, over the last 15 years another competent vector Aedes albopictus (Asian tiger mosquito) has been introduced into Europe and expanded into several countries, raising the possibility of dengue transmission (12).
Epidemiological studies have shown that temperature is a factor in dengue transmission in urban areas (13). Climate change projections on the basis of humidity for 2085 suggests dengue transmission to shift the latitudinal and altitudinal range (14). In temperate locations, climate change could further increase the length of the transmission season (15). An increase in mean temperature could result in seasonal dengue transmission in southern Europe if A aegypti infected with the virus were to be established.
Chikungunya fever is caused by a virus of the genus Alphavirus, in the family Togaviridae, which is transmitted to human beings by the bite of infected mosquitoes such as A aegypti, and A albopictus.
A confirmed outbreak of chikungunya fever was reported in August 2007 in northeastern Italy, the first chikungunya outbreak on the European continent (16,17,18). Vector surveillance in the vicinity of the cases identified large numbers of A albopictus mosquitoes in traps, but no sandflies or other vectors. While introductions of A albopictus and chikungunya virus into Italy were accidental events, a climatic model with five scenarios has been developed for possible further establishment of A albopictus in Europe with main variables such as mild winters, mean annual rainfall exceeding 50 cm and mean summer temperatures exceeding 20°C (19). Vector population density, an important determinant of the epidemic potential, is also linked to duration of the seasonal activity; therefore, the weeks between spring egg hatching and autumn egg diapause are also factored in. This model defines the potential for further transmission and dispersion of the vector under favourable climatic conditions in temperate countries and outlines the geographic areas potentially at risk of future outbreaks.
Malaria is caused by one of four species of the Plasmodium parasite transmitted by female Anopheles spp mosquitoes. Historically malaria was endemic in Europe, including Scandinavia, but it was eventually eliminated in 1975 through a number of factors related to socioeconomic development (20, 21). Any role that climate played in malaria reduction would have been small. Nevertheless, the potential for malaria transmission is intricately connected to meteorological conditions such as temperature and precipitation (22). For example, conditions for transmission in Europe have remained favourable as documented by sporadic autochthonous transmission of a tropical malaria strain by local vectors to a susceptible person (23, 24).
The potential for malaria and other “tropical” diseases to invade southern Europe is commonly cited as an example of the territorial expansion of risk due to climate change (socioeconomic, building codes, land use, treatment, capacity of health-care system, etc). Projections of malaria under future climate change scenarios are limited in Europe. An assessment in Portugal projected an increase in the number of days per year suitable for malaria transmission; however, transmission would depend on infected vectors to be present (25). For the UK, an increase in risk of local malaria transmission based on change in temperature projected to occur by 2050 was estimated to be 8 to 14%, but malaria re-establishment is highly unlikely (26). Thus, while climatic factors may favor autochthonous transmission, increased vector density, and accelerated parasite development, other factors (socioeconomic, building codes, land use, treatment, etc) limit the likelihood of climate-related re-emergence of malaria in Europe (27).
Leishmaniasis is a protozoan parasitic infection caused by Leishmania infantum that is transmitted to human beings through the bite of an infected female sandfly. Temperature influences the biting activity rates of the vector, diapause, and maturation of the protozoan parasite in the vector (28, 29). Sandfly distribution in Europe is south of latitude 45oN and less than 800 m above sea level, although it has recently expanded as high as 49°N (30 31). Historically, sand-fly vectors from the Mediterranean have dispersed northwards in the postglacial period based on morphological samples from France and northeast Spain and sandflies have been reported today also from northern Germany32. The biting activity of European sandflies is strongly seasonal, and in most areas is restricted to summer months. Currently, sandfly vectors have a substantially wider range than that of L infantum, and imported cases of infected dogs are common in central and northern Europe. Once conditions make transmission suitable in northern latitudes, these imported cases could act as plentiful source of infections, permitting the development of new endemic foci. Conversely, if climatic conditions become too hot and dry for vector survival, the disease may disappear in southern latitudes. Thus, complex climatic and environmental changes (such as land use) will continue to shift the dispersal of leishmaniasis in Europe (33, 34).
Tick-borne encephalitis (TBE) is caused by an arbovirus of the family Flaviviridae and is transmitted by ticks (predominantly Ixodes ricinus) that act both as vectors and as reservoirs (35). Similar to other vector-borne diseases, temperature accelerates the ticks’ developmental cycle, egg production, population density, and distribution. It is likely that climate change has already led to changes in the distribution of I ricinus populations in Europe (36). I ricinus has expanded into higher altitudes in the Czech Republic over the last two decades, which has been related to increases in average temperatures (37, 38, 39).
This vector expansion is accompanied by infections with TBE virus (40, 41). In Sweden, since the late 1950s all cases of encephalitis admitted in Stockholm County have been serologically tested for TBE (45). An analysis of the period 1960–98 showed that the increase in TBE incidence since the mid-1980s is related to milder and shorter winters, resulting in longer tick-activity seasons. In Sweden, the distribution-limit shifted to higher latitude ; the distribution has also shifted in Norway and Germany (43, 44).
Climate models with warmer and drier summers project that TBE will be driven into higher altitude and latitude, although certain other parts of Europe will be cleared of TBE (45). However, these climatic changes alone are unlikely to explain the surge in TBE incidence over the last three decades, and it is endemic in 27 European countries today (54). There is considerable spatial heterogeneity in the increased incidence of TBE in Europe, despite observed uniform patterns of climate change46. Potential causal pathways include changing land use patterns; increased density of large hosts for adult ticks (e.g. deer); habitat expansion of rodent hosts; alterations in recreational and occupational human activity (habitat encroachment); public awareness, vaccination coverage, and tourism (47, 48). These hypotheses can be tested epidemiologically and tackled through public-health action.
Lyme Borreliosis is caused by infection with the bacterial spirochete Borrelia burgdorferi which is transmitted to human beings during the blood feeding of hard ticks of the genus Ixodes. In Europe, the primary vector is I ricinus, also known as deer tick, as well as I persulcatus from Estonia to far eastern Russia. In Europe, Lyme borreliosis is the most common tick-borne disease with at least 85 000 cases yearly, and has an increasing incidence in several European countries such as Finland, Germany, Russia, Scotland, Slovenia and Sweden. Although detection bias could explain part of this trend, a prospective, population-based survey of cases in southern Sweden has serologically confirmed such an increase (49, 50).
A shift toward milder winter temperatures due to climate change may enable expansion of Lyme borreliosis into higher latitudes and altitudes, but only if all of the vertebrate host species required by tick vectors are equally able to shift their population distribution. In contrast, droughts and severe floods will negatively affect the distribution, at least temporarily. Northern Europe is predicted to experience higher temperature with increased precipitation while Southern Europe will become drier, which will impact tick distribution, alter their seasonal activity and, shift exposure patterns (51).
Crimean-Congo hemorrhagic fever (CCHF) is caused by an RNA virus of the Bunyaviridae family and transmitted by Hyalomma spp ticks from domestic and wild animals. The virus is the most widespread tick-borne arbovirus and is found in the Eastern Mediterranean where there have been a series of outbreaks in Bulgaria in 2002 and 2003, in Albania and in Kosovo in 2001 (52, 53, 54). Milder weather conditions, favouring tick reproduction may influence CCHF distribution (55). For example, an outbreak in Turkey was linked to a milder spring season (a substantial number of days in April with a mean temperature higher than 5°C) in the year before the outbreak. However, other factors such as land use and demographic changes have also been implicated. There have been new records of spotted fever group rickettsioses with new pathogens such as Rickettsia slovaca, R. Helvetica, Rickettsia aeschlimannii and flea-borne rickettsioses (Rickettsia typhi, Rickettsia felis) (57, 58). However, this emergence is most likely detection bias due to advancements in diagnostic techniques. Since ticks, flees, and lice serve as vectors as well as reservoirs they might contribute to disease amplification under favorable climate change conditions. There has been a geographic expansion of rickettsial diseases throughout Europe (59), and while underlying reasons for this expansion are still unclear, it is possible that wild bird migration could play a part (60).
Human Granulocytic Anaplasmosis is caused by Anaplasma phagocytophilum, a bacterium usually transmitted to humanbeings by I ricinus. In Europe, this disease was known to cause fever in goats, sheep, and cattle until it emerged as a disease in human beings in 1996 (61). It has now shifted to new geographical habitats throughout Europe, and migrating birds have been implicated in its expansion (62). Spatial models have been developed to project the geographical distribution under climate change scenarios for North America but not for Europe (63, 64).
Based on the vector-borne disease articles reviewed, here it is clear that climate is an important geographic determinant of vectors, but the data do not conclusively demonstrate that recent climatic changes have resulted in increased disease vector-borne disease incidence on a pan-European level. However, the reports indicate that under climate change scenarios of the last decades ticks have progressively spread into higher latitudes in Sweden and higher elevation in the Czech Republic; they have become more prevalent in many other places and intensified the transmission season. Conversely, the risk for Lyme borreliosis is projected to be reduced in drought and flood-ridden locations. The articles reviewed here do not support the notion that climate change has altered the distribution of sandflies and visceral leishmaniasis but since sandfly vectors expand further than L infantum this hypothesis cannot be discounted. The risk of reintroduction of malaria into certain European countries is very low and determined by other variables rather than climate change. Introduction of dengue, West Nile fever, and chikungunya into new regions in Europe is a more immediate consequence of virus importation into competent vector habitats; climate change is one of many factors that influence vector habitat.
The lack of published articles for other vector-borne diseases makes an assessment difficult; for example, tick-borne relapsing fever caused by spirochaetes of the genus Borrelia could spread from its current endemic area in Spain since its tick vector is sensitive to climatic changes but no climate models have been developed for this disease (65). In the case of yellow fever the existence of an effective vaccine makes the establishment in Europe very unlikely; conversely, an existing human vaccine for Rift Valley fever is not available (veterinary vaccines are used in Africa). These multifactorial events call for a case by case assessment and targeted interventions.
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