Review

Dengue and dengue vectors in the WHO European region:

past, present, and scenarios for the future
Francis Schaffner, Alexander Mathis

After 55 years of absence, dengue has re-emerged in the WHO European region both as locally transmitted sporadic Lancet Infect Dis 2014;
cases and as an outbreak in Madeira, driven by the introduction of people infected with the virus and the invasion of the 14: 1271–80

vector mosquito species Aedes aegypti and Aedes albopictus. Models predict a further spread of A albopictus, particularly Published Online
August 27, 2014
under climate change conditions. Dengue transmission models suggest a low risk in Europe, but these models too
http://dx.doi.org/10.1016/
rarely include transmission by A albopictus (the main established vector). Further information gaps exist with regard to S1473-3099(14)70834-5
the Caucasus and central Asian countries of the WHO European region. Many European countries have implemented Institute of Parasitology, Swiss
surveillance and control measures for invasive mosquitoes, but only a few include surveillance for dengue. As long as National Centre for Vector
no dengue-specific prophylaxis or therapeutics are available, integrated vector management is the most sustainable Entomology, University of
Zurich, Zurich, Switzerland
control option. The rapid elimination of newly introduced A aegypti populations should be targeted in the European
(F Schaffner PhD, A Mathis PhD)
region, particularly in southern Europe and the Caucasus, where the species was present for decades until the 1950s.
Correspondence to:
Dr Alexander Mathis, Institute of
Introduction In this review, we aim to describe dengue in the Parasitology, National Centre for
Dengue is the most rapidly spreading mosquito-borne context of the European region. We have compiled data Vector Entomology, University of
Zurich, Winterthurerstr 266a,
disease, with a 30-fold increase in global incidence during for the historical and present occurrence of dengue and
8057 Zurich, Switzerland
the past 50 years, affecting more than 100 countries the incriminated mosquito vectors in this region, and alexander.mathis@uzh.ch
throughout tropical and subtropical regions of the world.1 summarised models and risk maps of dengue and its
However, no concerted action has been taken against vectors as well as surveillance and risk plans in the
dengue. WHO has defined a global strategy for dengue European region. WHO’s European region includes
prevention and control, 2012–20,1 aimed at reduction of the 53 Member States, including geographical Europe and
burden of this disease. WHO estimates that 50–100 million its outermost regions (but not associated overseas
dengue infections occur every year, but a recent model2 territories), Russia, Turkey, Israel, countries in the
suggests that this figure is a substantial underestimation. Caucasus (Armenia, Azerbaijan, and Georgia), and
Important drivers for dengue transmission dynamics are countries in central Asia (Kazakhstan, Kyrgyzstan,
socioeconomic factors, including globalisation (rapid Tajikistan, Turkmenistan, and Uzbekistan).
movement of people infected with the virus and com-
petent mosquito vectors), urbanisation (high density of Outbreaks of dengue in the WHO European region
susceptible people, plethora of mosquito breeding sites),2 The early history of dengue is unclear because of the
and climate factors (eg, the capacity of mosquitoes to similarity of its clinical picture to other febrile illnesses.
transmit the virus is heavily dependent on temperature). Dengue was recognised as a specific disease entity in
Although nearly 75% of the global population exposed human beings in the late 18th century. However, many
to dengue is in the Asia-Pacific region, the WHO cases were probably confused with chikungunya,
European region is also affected. The 2010–13 reports of another arboviral disease transmitted by A aegypti.14 In
autochthonous cases in France and Croatia3–6 and the 1903, Graham hypothesised dengue was transmitted by
outbreak in Madeira7,8 are reminiscent of endemic or mosquitoes,37 and Bancroft confirmed this in 1906.38 A
epidemic dengue that affected many countries of the scientific literature search of dengue in the WHO
eastern hemisphere until the 1930s. At that time, the European region showed that several epidemics occurred
principal mosquito vector Aedes aegypti was endemic in during the 18th and 19th centuries, in ports of the
parts of southern Europe, and several outbreaks of dengue eastern Mediterranean (table) but also occasionally
arose in areas where this mosquito was established (table). inland (eg, in the cities of Andalusia in Spain and in
Subsequently, 13 southern Mediterranean and Caucasian Greece).10,11,21 At that time, the vector A aegypti was
countries agreed on an “international convention for repeatedly introduced into ports by vessels and was
mutual protection against dengue fever” in 1935,30,31 to widely established in southern Europe, which fuelled
limit the possible spread of dengue. Nowadays, concern yellow fever outbreaks in port cities and occasionally
about dengue and other tropical arbovirus infections such their hinterlands (eg, Barcelona, Lisbon, and Seville) in
as chikungunya is rising in the European region, driven the 19th century.39,40 The largest and almost last dengue
by several factors including the resurgence of A aegypti, outbreak in the Mediterranean (Greece and Turkey)
the widespread establishment of another efficient vector occurred in 1927–28, affected more than 1 million people
(Aedes albopictus), the increase in the number of pathogen (90% of the population in Athens), and killed
introductions by tourism and migration, the reports of 1000–1500.18,41 No historical dengue virus transmission
local outbreaks, and predicted environmental changes is known from eastern Russia or from the Caucasus and
including climate change.32–36 central Asia.42

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 Review

Location Notes
1784, 1788, 1793 Cadiz, Seville (Spain)9,10 End of first pandemic, 1779–84
1861 Cyprus11 ··
1863, 1867 Cadiz (Spain), then Jerez, Seville, and other places in Andalusia10,11 Imported from the West Indies by troops
1865 Canary Islands (Spain)10 ··
1881 Crete (Greece)11–13 Half of the inhabitants affected
1887 Gibraltar10 Fifth pandemic, 1887–89
1888–1889 Cyprus10 ··
1889 Athens, Piraeus, Salonica (Greece),13,14 Greek Islands (Rhodes, Chios, and others), Around 80 000 cases in Izmir (80% of the inhabitants)
southern Turkey,10,11,16 Izmir,15 Manisa to Istanbul, Trabizon (Turkey),
Varna*(Bulgaria), Lisbon (Portugal), Israel10,11,16
1889–1890 Istanbul, Izmir (Turkey), Napoli (Italy)9,11,17 ··
1895–1897 Athens (Greece)14 ··
1899 Antalya (Turkey)11 ··
1910 Athens, Piraeus (Greece)12,16,18 ··
1912 Israel19 ··
1913 Cyprus11 ··
1916 Dardanelles, Trabizon (Turkey)11,20 ··
1921 Vienna*(Austria)21 ··
1927 Malta16 ··
1927–1928 Piraeus, Athens, Euboea, Gulf of Aegina (Greece), Izmir to south of Rhodes More than 1 million of people affected (90% of the
(Turkey)10,13,21, Israel16, Greece: DEN-1 and DEN-2 confirmed by retrospective population in Athens); 1000–1500 deaths
serological study22,23
1928 Cyprus, Andalusia24,25 ··
1929 Izmir25 ··
1929–1933 Greece22,26 Confirmed by retrospective serological study
1945 Turkey, Israel (and other Middle East countries)27 ··
2010 Croatia;3,5 three DEN-1 clinical cases (including one reported in Germany) plus Virus probably introduced from Indian subcontinent
15 recent infections
2010, 2013 France;4,6 DEN-1 cases (2010), one DEN-2 case (2013) Viruses probably introduced from West Indies
2012–13 Madeira;7,8,28 more than 2200 DEN-1 cases from October, 2012, to January, 2013, Virus probably introduced from Venezuela29
plus 74 cases reported from Portugal mainland8 and 12 other European countries

DEN-1=dengue virus serotype 1. DEN-2=dengue virus serotype 2. *Not clear whether data refer to a dengue outbreak or imported cases only, as there is no indication for the
presence of A aegypti in Varna and Vienna.

Table: Historical and contemporary outbreaks of dengue in the WHO European region

For more on A albopictus global
invasion see www.issg.org/
database/welcome
Dengue fever has been an imported disease in the
European region during the past few decades. As many
as 1143 confirmed cases were reported by the European
Union or European Economic Area countries in 2010,
rendering dengue the second most frequent reason, after
malaria, for admission to hospital after return from
abroad.43 Few autochthonous dengue virus transmissions
were reported in 2010 from France (two cases) and Croatia
(17 cases3). However, a large outbreak occurred in the
Portuguese autonomous region of Madeira, with more
than 2200 confirmed cases between October, 2012, and
January, 2013, and an additional 78 cases were reported in
European travellers returning from the island.8 Finally,
one case was reported in southern France in October,
2013.6 These autochthonous dengue cases in the
European region were caused by the arrival of people
infected with the virus, the establishment of efficient
mosquito vector species (ie, A albopictus in France and
Croatia and A aegypti in Madeira), and a high population
density of immunologically naive people.44
The main dengue vectors A aegypti and
A albopictus in the WHO European region
Origins
The main (urban) vector worldwide A aegypti (figure 1)
originated from west Africa and was dispersed to tropical
or subtropical areas of other continents on vessels with
the slave trade and other trade routes.45 A albopictus
(figure 1), native to southeast Asia and invasive in many
countries, is generally regarded as the secondary vector
but has been incriminated as the main dengue virus
vector in many disease outbreaks worldwide.46,47 The
larval habitats of both invasive species are natural water
bodies, such as tree holes and man-made water
containers (figure 2).
A aegypti
There is evidence that A aegypti reached Europe before the
end of the 17th century, when the first outbreaks of yellow
fever, for which it is also a vector, were reported in France
and Spain.39,48 We created a schematic historical distribution

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map of A aegypti (figure 3) based on consistent reports
with localities and dates of collection from the literature.
By the 1950s, the species was established in almost all
Mediterranean countries and around the Black Sea and
east to the Caspian Sea, which included both coast and
inland areas.21,42,45,49–54 From these records, the species never
established north of latitude 44°30’N. Yellow fever
outbreaks in port cities in more northerly areas (eg, Saint-
Nazaire, France, 1861, and Swansea, UK, 1865)49 were
triggered by the arrival of sailors infected with the virus
and the introduction of A aegypti, which could thrive locally
during the summer months. After the 1950s, A aegypti
seemed to disappear from the Mediterranean area.17
Between 1960 and 2000, A aegypti was incidentally reported
once from Italy (1972)55 and from Israel (1974),56 and
sporadically from Turkey (1961, 1984, 1992, 1993, 2001;
figure 3), without evidence of well established populations,
although these findings suggest the persistence of small
populations in Turkey.54,57 However, the species has
established in Madeira in 200458 and has again populated
the northern coast of the Black Sea (Russia and Georgia) in
2008.59 The temperature thresholds for the persistence of
A aegypti populations are thought to be the January
isotherm of 10°C53,60,61 or the annual mean of 15°C.62
Furthermore, eggs of A aegypti have a high mortality when
exposed to frost, which might occur at the cool margin of
its geographical distributions only during severe winters.62
There is only one study in which a regional European
risk map for A aegypti has been developed63 (appendix).
Coastal regions of the Mediterranean, Black, and Caspian
seas, and areas along large lowland rivers (Ebro, Garonne,
Rhone, and Po) were identified as suitable habitats for
A aegypti. The spread of A aegypti in the Black Sea region
strongly advocates to strengthen communication and
collaboration within the whole European region as has
already been achieved in the European Union under the
umbrella of the European Centre for Disease Prevention
and Control (ECDC).
A albopictus
Details of the history of the invasive mosquito A albopictus
in Europe are given elsewhere,64,65 and updated distribution
maps are available. By the end of 2013, A albopictus was
widely established and spreading in the western
Mediterranean basin, from Spain to Greece. Its presence
is also confirmed around the Black Sea coast (Bulgaria,
Romania, southern Russia, and Turkey). The distribution
map provided by the ECDC is based on data from the
European Network for Arthropod Vector Surveillance for
Human Public Health (VBORNET) that seem complete
and updated because we identified no additional data in
our scientific literature search. Incursions of A albopictus
have been reported in more northern countries, but no
establishment has been confirmed to date.
Several series of maps have been generated to anticipate
the future distribution of A albopictus in the European
region (appendix). The metrics applied in these models
www.thelancet.com/infection Vol 14 December 2014
Review
A B
F Schaffner, University of Zurich.
Figure 1: Aedes aegypti, adult female (A), and Aedes albopictus, adult female (B)
and the threshold values used were annual mean
temperature of 11°C, 1350 growing degree-days (measure
for heat accumulation), average annual precipitation of
500 mm, summer average temperature of 15–30°C
(optimum 20–25°C), and January mean temperatures of
0°C.66–70 However, data showed that mean January
temperature, annual mean temperature, and annual
precipitation were lower in newly invaded areas.71,72 All
generated maps suggest that in particular coastal areas
of Mediterranean countries, and to a lesser extent of the
eastern Black Sea, are suitable for A albopictus. Central
Europe and the inland Balkan region seem less suitable,
except in one model.63 When applying climate change
scenarios released by the Intergovernmental Panel on See Online for appendix
Climate Change (IPCC, 2007),73 all models suggest a
slight decrease of suitability in southern Europe, but an
increase of the suitability of central Europe and, with
some delay, of eastern countries. However, these models
neither include the effects of cold spells (A albopictus
eggs have a high mortality when exposed to temperatures
below –7°C74) nor can they predict transient summer
expansions. Additionally, there is a gap in the risk
mapping of the Caucasus and central Asian countries.
Other potential mosquito vector species
The major vectors (A aegypti and A albopictus) are
mosquitoes of the subgenus Stegomyia, which contains For more on distribution maps
other species present in the WHO European region see http://www.ecdc.europa.eu
including Aedes cretinus (distributed in Crete, Greece
mainland, Turkey, Black Sea coast of Ukraine, Russia,
and Georgia)42,75 and Aedes galloisi, Aedes flavopictus, and
Aedes sibiricus (in far-eastern Russia only).42,76 Whether
these species could act as vectors is unknown because
none of them have been subjected to experimental
infection. However, A cretinus, if competent, might have
contributed to virus transmission during the severe
outbreaks in Greece and Turkey (table).
Aedes japonicus (subspecies japonicus) originated from
Asia and was introduced into Europe. It has rapidly
dispersed in central Europe and proved to have a high
vector competence when tested in the laboratory.77
Additionally, it shows a pronounced anthropophilic
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The anthropophilic Aedes vittatus is occasionally

A mentioned as a vector of dengue virus in India,10,79,80
but because of its restricted larval habitats (water-fi lled
rock pools) and low distribution in Europe (western
Mediterranean), 75,81 its role as dengue virus vector is
likely to be very restricted.

Factors that determine the vectorial role

Many factors define the vectorial capacity (C) of a
mosquito population—(ie, its efficiency to act as a vector
in the field), shown by the equation C=bma²pn/–ln p,82
where b is the vector competence, (ie the proportion of
vectors in which infective pathogen stages develop); m is
the vector density; a is the vector’s daily blood-feeding
B rate on a host species; p is the vector’s daily survival rate;
and n is the time in days for the pathogens to reach the
saliva (extrinsic incubation period [EIP]).
The vector competence (b) is similar in A aegypti and
A albopictus.83–85 However, A aegypti is the epidemic vector
of the dengue virus because A aegypti females also bite
indoors and almost exclusively bite people. Furthermore,
they feed multiple times during a gonotrophic (egg
-producing) cycle.86 Subsequently, they attain distinctly
higher values of a than does A albopictus, which feeds on
blood only once per gonotrophic cycle and is thought to
be a generalist outdoor feeder.46,87 However, predominant
feeding on people for A albopictus has been reported
from some European cities (Barcelona and Rome).88,89
C
Population densities (m) of A aegypti generally seem to be
low.90,91 By contrast, A albopictus can be very abundant,
causing biting nuisance.92 A albopictus was the in-
criminated vector of dengue outbreaks in Hawaii at
places with high abundances where up to 90 biting
mosquitoes per person were counted in 5 min.93
Dengue virus development in the mosquito vector (EIP,
n) was estimated to be 15 days at 25°C and 6·5 days at
30°C in a model in which data from eight studies
investigating realistic transmission from viraemic to naive
hosts were used.94 Another model of dengue virus trans-
D mission estimated 28°C as the optimum temperature for
transmission.95 In Australia, dengue epidemics were
recorded only at average temperatures above 20°C, ceasing
at 14°C.96 All these temperature estimates nearly exclusively
refer to dengue virus transmission by A aegypti.
F Schaffner, University of Zurich.

Models and risk maps for dengue

Figure 2: Typical larval habitats of container-breeding Aedes spp in Europe.
Natural sites: tree hole (A) and rock pool (B). Man-made sites: vases and flower pot
dishes (C) and catch basin (D).
behaviour and high abundance in urban or suburban
environments. Therefore, A japonicus is a potential
dengue virus vector.78
During the past few years many studies have modelled
dengue risk at a global, regional, or local scale, with
evidence-based consensus mapping, spatial modelling,
and other modelling techniques.2,63,95,97–106 Some models
have been reviewed,26,107–109 and those producing risk
maps for Europe are discussed in the appendix.
Dengue transmission dynamics are driven by climate
factors and socioeconomic factors. Socioeconomic
factors were considered only recently in two reports.2,106
Most of the models investigated the distribution of
dengue through the association between the vector or

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 Review

the pathogen and the environment, and the possible

changes due to climate changes (mainly temperature) A Sporadic records in ports
Established populations
were modelled and projected. However, associations No data
between climate variables (temperature, rainfall, and
humidity) and dengue virus transmission are highly
complex.90,110,111 General shortcomings of models are their
sensitivity to temporal and spatial heterogeneity, the
stochasticity of many metrics, the restricted availability
of data, and the still insufficient understanding of the
effects of factors on the occurrence of the disease.107,112
Under present conditions, Europe still seems to be
at low risk of dengue virus transmission.63,106 Biological
models based on vectorial capacity show that dengue
virus transmission is possible in Greece, but only
during summer months, and an increased risk is
predicted for various climate change scenarios.97,98
Empirical models suggest temperate regions are free
of risk, and a global increase of populations to be at B Sporadic records (NUTS3)
risk under climate change scenarios.100,101 Indeed, parts Established populations (NUTS3)
No data
of the Mediterranean are projected to be at a greater
risk, with some parts of central Europe becoming
suitable for virus amplification within A aegypti, which
was shown by a model exploring the association
between temperature and the extrinsic incubation
period.104 Modelling of environmental distance also
suggests that large areas of Europe are quite similar to
southern USA where dengue has occurred in 2009–10
and in 2013.106 Integration of human population
density into such models suggests that more areas are
suitable for dengue virus spread (ie, major towns and
cities106) but the predicted suitability is likely to be an
overestimation, especially in areas where temperature
needs for dengue virus amplification in vectors are not Figure 3: Distribution of Aedes aegypti in the WHO European region.
met.104 Models analysing environmental distances are Historical distribution up to 1960 (A) and contemporary distribution. (B) Data shown as territorial unit NUTS/
based either on transmission mediated by A aegypti nomenclature of territorial units for statistics, level 3, source ECDC/VBORNET database (small areas encircled).
only,63 or on a few outbreaks mediated by A albopictus.106

Dengue surveillance and risk plans in the WHO
European region
Programmes to prevent or reduce the burden of dengue
and chikungunya in Europe have existed since 2006,
after a dramatic increase of chikungunya virus
circulation was reported from the Indian Ocean and
Asian territories. Because of strong connections with
such territories (overseas territories), the chikungunya
outbreak in Reunion led France to adopt a national plan
for its mainland to prevent the dissemination of both
chikungunya virus and dengue virus.4,113 A national
mosquito control programme existed from 2000 to 2005,
aiming to survey introductions of A albopictus and
prevent its establishment by immediate application of
control measures. In 2006, this programme evolved into
an integrated surveillance programme combining
surveillance and control of both vector and disease.
Thus, surveillance measures of dengue and chikun-
gunya cases (both introduced and autochthonous) and
application of focal vector control measures around such
cases and in areas where A albopictus is established and For more on the distribution of
active were added. All these measures, together with Aedes aegypti in the WHO
European region see http://
other complementary measures such as public ecdc.europa.eu/en/healthtopics/
information about mosquito bite prevention, are applied vectors/vector-maps/Pages/
according to risk that is based on both vector occurrence VBORNET_maps.aspx
and virus circulation. Such an integrated plan supports
preparedness and allows rapid implementation of
adapted responses. Although several European countries
have implemented surveillance and control measures
for invasive mosquitoes, integrated plans (comprising
surveillance and control of both vector and disease) exist
only at regional level in Italy (since 2008) where
chikungunya virus was locally transmitted.113 Addition-
ally, Switzerland has drafted a national plan, but the
control programme is effective in only one canton
(Ticino). Belgium is also developing a plan, following
the recommendations of the ECDC guidelines for the
surveillance of invasive mosquitoes in Europe.114 These
guidelines provide support for the implementation of
tailored surveillance of invasive mosquito species as

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 Review
part of the control of mosquito-borne diseases, including
integrated vector control, among other methods to
manage mosquito-borne disease risks in Europe.
Discussion
The high efficiency of A aegypti in the transmission of
dengue virus has been shown once again by the dengue
outbreak in Madeira, which occurred only 6 years after
the first appearance of this mosquito species on the
island. The mosquito population in Madeira is a
possible source for repeated introductions to Portugal
via the biweekly ferry traffic or the plant and flower
trade.58 A aegypti might also spread along the Black Sea
coast. There are no predictive models with regard to a
potential distribution of A aegypti under climate change
scenarios. Historical data show that A aegypti was
widespread in southern Europe, then seemingly
disappeared. Re-introductions are continuously occur-
ring, as shown in the Netherlands where A aegypti
temporarily reproduced in a used tyre yard, after its
import from the USA.115 Of particular interest, however,
is the disappearance of historical dengue and A aegypti
in the WHO European region and whether this was an
effect of mosquito control measures. Vector control
measures along the northeastern Black Sea coast51 were
implemented in the wake of the large dengue outbreak
in Greece in 1927–28. These measures resulted in a
sustained reduction of the mosquito as “it has not been
found there in recent years”.42 Few targeted control
campaigns directed towards A aegypti have been
implemented in the Mediterranean area. Two main
Panel: Challenges related to dengue in the WHO European region
• Models imply that geographical Europe is at low risk of dengue transmission, but no
such models are available for the other parts of the European region.
• Models focus on climatic metrics as key drivers for dengue virus transmission.
Environmental (eg, land use) and socioeconomic factors, which also affect
transmission in complex interactions, have been considered only in the most recent
models. All developed risk maps rely heavily on Aedes aegypti-transmitted dengue, but
Aedes albopictus might be the relevant vector in most of the European region. No
model exists on the potential distribution of transmission by A aegypti under climate
change scenarios.
• Surveillance and control programmes for dengue vectors exist in several European
countries, but only few also include the disease. Integrated programmes should be
generalised, at least in southern Europe and the Caucasus where the highly efficient
vector A aegypti was present for decades until the 1950s, and where proactive
surveillance of this species with rapid elimination should be the aim. A albopictus,
predicted to spread particularly under climate change conditions, is an efficient vector
when highly abundant or under conditions that favour anthropophilic feeding
behaviour (cities), and mosquito populations should be suppressed under these
conditions. Awareness for other potential mosquito vectors of dengue virus (native,
invasive) thriving in the European region should be created.
• As long as no dengue-specific prophylaxis or therapeutics are available, sustainable
vector management is the only available approach for prevention and control. Novel
mosquito control methods are being developed and merit further support without delay.
1276
causes are widely proposed for the disappearance of the
A aegypti species. First, piped water supply systems
reduced the availability of larval habitats, which was
probably the major factor in the range contraction of
this species in Australia.96 Second is the wide application
of DDT (dichlorodiphenyltrichloroethane) in residual
sprayings for malaria mosquito control operations,
which also affected A aegypti.17,54 However, natural
extinction was also reported in areas where these
conditions did not apply.17
Another vector species, A albopictus, is spreading in
Europe and has substantial potential to further expand
its range because of its overwintering capabilities in
temperate climates and in the context of climate change
as predicted in several models. Generally, A albopictus
plays a minor part in global dengue epidemics but has a
proven high vectorial capacity in some contexts. The
conceivable (but unpredictable) emergence of dengue
virus lineages adapted to enhanced transmission by this
species might substantially change the dengue risk.
Further, dengue virus has adapted to the peridomestic A
albopictus in Asia and to what is nowadays thought to be
the main vector species A aegypti, which originates from
Africa,83,116 and might in the future exploit other mosquito
species as a vector.117,118
Models show that Europe has a low risk of dengue
transmission, although managing dengue risk remains
challenging (panel). Travel-related or migration-related
influx of dengue virus into the European region, however,
will continue to increase as long as the dengue situation
worsens in endemic countries.119 When the virus originates
from an infected patient, secondary transmission is
possible in areas where a vector is established, at least
during summer. Large parts of Europe have high summer
temperatures and environmental characteristics similar to
those of the dengue endemic subtropical and tropical
areas.40,106
Most biological models use only temperature as a
climatic variable to show and quantify the effect of
possible changes,97,98 whereas rainfall (and water storage)
might also have an effect. Other limitations are the low
number of metrics used for vectorial capacity, and not
enough consideration given to other variables and to
local conditions. These factors include social factors,
health services, virus reservoir, mosquito densities, virus
introduction and synchronicity with high vector density,
human population susceptibility, indirect effects of
climate change on human and mosquito population, and
demographical changes. Most of the empirical models
account for interactions between climatic variables100 but
do not consider the local variables. A larger panel of
predictor variables has been used in a biological model,
including vegetation or moisture, urbanisation, urban
accessibility, and relative poverty, besides precipitation
and temperature variables.2 However, all models are
based on reports of dengue cases, which are known to
underestimate the disease, particularly in African
www.thelancet.com/infection Vol 14 December 2014

countries1,105 and also use pseudoabsence points rather
than recorded absences.63,106
New data sources and computer techniques contributed
to increase the resolution of climate datasets and map
outputs, and subsequently to produce regional risk maps
for Europe.63,106 However, a biological gap exists because all
models rely heavily on transmission by A aegypti, whereas
A albopictus might be the vector in most of the WHO
European region. Additionally, a geographical gap exists
in that the current models do not cover the Caucasus and
central Asian regions and most parts of Russia. Thus, the
area is being further explored with ongoing projects of
three European dengue research consortia.120
As long as neither vaccines nor specific treatments
(antiviral drugs, therapeutic antibodies) are available,121–123
two types of measures can be implemented to reduce the
burden of dengue:1 stopping of the invasion of efficient
vector mosquitoes; and diagnosis of disease early,
improved case management, and active disease sur-
veillance leading to enhanced outbreak preparedness.
However, early diagnosis can be compromised because
the proportion of unapparent (asymptomatic) cases can
vary from 50% to 90%.124
Control of dengue vectors needs vector surveillance and
sustainable integrated vector control. Commonly applied
control measures vary little from those applied 60 years
ago, except for the use of modern insecticides. The focus
on elimination of larval habitats includes community
participation (eg, properly disposing of solid waste and
removal of artificial man-made water containers; covering,
emptying, and cleaning of domestic water storage
containers on a weekly basis) and application of larvicides
or predators.125–127 Effectiveness of spatial spraying with
adulticides against adult dengue virus vectors is poorly
assessed,128,129 but is still included in emergency responses.4
Experience has suggested that contact insecticides applied
inside dwellings might be effective.130 Newly established
populations of A albopictus could be eliminated in some
places (France, Netherlands) by the rapid implementation
of targeted control measures (a combination of spraying
with larvicides and adulticides).64,131 However, elimination
is almost impossible once the species is established, at
least in southern Europe.64,132 The control of A aegypti and A
albopictus is complex and needs to involve the community
with public health education, the modification of human
behaviour, and adaptation of legal regulation (to enforce
control measures).60,65,133–135 The use of insecticides, a
reduction in potential breeding sites, and an increase in
public health awareness has thus far not eliminated the
established A aegypti population in Madeira;58 however, the
disappearance of the species from continental Europe in
the 1950s, in some cases after the implementation of
control measures, suggests that elimination is achievable
at some places. Novel complementary measures include
many recently developed and field-tested approaches (for
both A aegypti and A albopictus). These approaches include
sterile-insect methods,136–138 mosquito growth regulator
www.thelancet.com/infection Vol 14 December 2014
Review
Search strategy and selection criteria
We identified references for this review through searches on
OvidSP (including BIOSIS Previews and Ovid MEDLINE), CAB
direct, and Web of Science, in any language between 1900 and
February, 2014. Search terms were defined according to five
search strings: (1) past, current, and future distribution of
Aedes aegypti and Aedes albopictus in countries of the WHO
European region; (2) identification of other potential
mosquito vector species; (3) outbreaks of dengue in the
European region; (4) models and risk maps for dengue; and (5)
dengue surveillance and risk plans in countries of the European
region. We identified additional references by snowballing and
reference tracking, which was particularly relevant for old
papers (distribution data for A aegypti and dengue outbreaks)
and grey literature.
transfer that exploits adult mosquitoes to disseminate a
substance that disrupts larval development to breeding
sites,139,140 and the application of mosquito-specific
pathogens.141 Additionally, the use of transinfected
endosymbiotic bacteria of the genus Wolbachia limited the
transmission of dengue virus.142 Finally, other alternatives
to control disease transmission consist of reduction of the
human—vector contact through the use of insect repellents
and insecticide-treated materials (eg, clothes and screens),
which remains the main and most effective control
measure in endemic developing countries. Of paramount
importance is that measures must be adapted to the local
circumstances. In the context of the European region,
effective dengue prevention and control depends on the
prompt response to introduced cases, whatever the applied
measures are.
Contributors
FS did the literature search and edited the table and figures. FS and AM
extracted and interpreted the data and wrote the manuscript.
Declaration of interests
We declare no competing interests.
Acknowledgments
This work was commissioned and partly financed by WHO Regional
Office for Europe, Climate Change and Sustainable Development
Program coordinated by Bettina Menne, with support by the German
Federal Ministry for Environment, Nuclear Safety and Nature Protection.
We thank Bettina Menne for her text contributions throughout the
development of the paper, and critical comments from Maha Bouzid
(University of East Anglia), Mikhail Ejov (WHO), Raman Velayudhan
(WHO), Jan Semenza (ECDC), Wim Van Bortel (ECDC), Hervé Zeller
(ECDC), Norbert Becker (KABS), and William Wint (ERGO). Additionally,
we thank Paul Torgerson (University of Zurich) for linguistic revision.
We acknowledge ECDC and VBORNET experts for providing vector
distribution data, and the Swiss Federal Food Safety and Veterinary Office
as sponsor of the Swiss National Centre for Vector Entomology.
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