HAZARDS ASSOCIATED WITH MOSQUITO SPECIES
Aedes aegypti was previously found sporadically in Europe in the first half of the 20th century as far north as Brest and Odessa, but it disappeared from the Mediterranean region due to reasons unknown . It has since re-colonised Madeira  and parts of Southern Russia and Georgia (Krasnodar Krai and Abkhazia ) and has been recently reported in the Netherlands , making it one of the most widespread mosquito species globally. There are no climatic reasons why Ae. aegypti, if introduced into Europe, could not survive across southern Europe. If this were to happen, it may increase the risk of disease transmission of yellow fever virus and dengue virus . Although its global establishment is currently restricted due to its intolerance to temperate winters , over the past 25 years there has been an increase in its distribution worldwide .
The success of this invasive species has largely been due to globalisation. It thrives in densely populated areas which lack reliable water supplies, waste management and sanitation . Historically, Ae. aegypti has moved from continent to continent via ships, and this method of dispersal is thought to present the highest risk of introducing this mosquito into continental Europe from Madeira. It is suggested that Ae. aegypti evolved its domestic behaviour in West Africa and its widespread distribution and colonisation in the tropics led to the highly efficient inter-human transmission of viruses such as dengue . This domestic behaviour can provide protection against environmental conditions (as it rests indoors) and numerous habitats suitable as oviposition sites, but can also result in increased sensitivity to control measures used to eliminate them .
Biting and disease risk
Aedes aegypti is a known vector of several viruses including yellow fever virus, dengue virus and chikungunya virus. Hundreds of imported cases are reported in Europe every year, including fatal cases . Therefore the establishment of this mosquito in Europe raises concerns about autochthonous arbovirus transmission , particularly in southern Europe where climatic conditions are more suitable for the re-establishment of this species. In 2012, a large outbreak of dengue fever occurred in the Portuguese Autonomous Region of Madeira  associated with Ae. aegypti. The epidemic started in October 2012 and by early January 2013 more than 2 000 cases of dengue fever had been reported, with an additional 78 cases reported among European travellers returning from the island .
Aedes aegypti was previously been reported from Crete, Cyprus, France (incl. Corsica), Greece, Israel, Italy, Portugal, Southern Russia, Sardinia, Spain, Syria, Turkey and the former Yugoslavia in Europe and the Middle East and Algeria, Egypt, Libya, Morocco and Tunisia in North Africa . It is currently distributed in Africa, the surrounding tropics and subtropics, south eastern US, the Middle East, South East Asia, Pacific and Indian Islands and Northern Australia . Although historically present in Europe, recent reports of its presence have come from Madeira, the Netherlands and the north-eastern Black Sea coast (southern Russia and Georgia).
Brief history of spread and European distribution
Aedes aegypti were most likely transported into the Americas and the Mediterranean on sailing ships from Africa [1,7,14]. Historically, Ae. aegypti were reported sporadically in Europe from the Atlantic coast (Britain, France, and Portugal) to the Black Sea, displaying a much larger distribution compared to its current one. The same applies to North America and Australia . This reduction was possibly due to eradication programs.
Initial importations and spread in Europe
Since historical reports of the presence of Ae. aegypti in Europe, it is only more recently that reports of re-colonisation have come to light. It was reported in the UK in 1919 and Brittany in France . It was reported in Spain up to 1953, Portugal up to 1956 and Madeira up until 1977–79, and its sporadic presence has been reported in Britain, France, Malta, Italy, Croatia, Ukraine, Russia and Turkey . Re-colonisation was reported from the island of Madeira in 2004 and 2005. Aedes aegypti is now established on the island and there are concerns that it could be transported to western continental Europe via air or sea traffic . For Eastern Europe there are concerns that it could be introduced from Russia and Georgia (Abkhazia) to other countries bordering the Black Sea via road or sea traffic. It was more recently reported in the Netherlands at tyre yards. It is thought to have been imported into the country via a shipment of tyres from Florida, USA [3, 16].
Possible future expansion
Unlike Aedes albopictus, the ability for Ae. aegypti to establish in more temperate regions is currently restricted due to its intolerance to temperate winters  but it could become widely established again in the Mediterranean and this could change in the future with global climate change resulting in northern and southern expansion of Ae. aegypti .
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Species name/classification: Aedes aegypti (Linnaeus)
Common name: Yellow fever mosquito
Synonyms and other name in use: Stegomyia aegypti 
Morphological characters and similar species
Adults of Ae. aegypti are relatively small and show a black and white pattern due to the presence of white/silver scale patches on a black background on the legs and other parts of the body. Some indigenous mosquitoes also show such contrasts (more brownish and yellowish) but in those cases it is less obvious. However Ae. aegypti could be mixed up with other invasive (Aedes albopictus, Aedes japonicus) or indigenous species (Aedes cretinus, restricted to Greece and Turkey), and the diagnostic character is the presence of silver scales in a shape of a lyre on a black background on the scutum (dorsal part of the thorax). The domestic form (Aedes aegypti aegypti) is paler than its ancestor (Aedes aegypti formosus) and has white scales on the first abdominal tergite  .
Adults peaked in February, May–June, and again in September, during a study in Parque des Dunas de Natal, Brazil. During the same study, increasing numbers of eggs were found during February and again in July with larval densities peaking one month later . Previous studies have shown populations of Ae. aegypti to remain active in Egypt throughout winter, in Spain from the summer through to December, in Morocco in October and December and in Algeria up to the end of the summer and early winter .
Voltinism (generations per season):
Host preferences (e.g. birds, mammals, humans):
Aedes aegypti prefer mammalian hosts  and will preferentially feed on humans, even in the presence of alternative hosts . They also feed on multiple hosts during one gonotrophic cycle [5, 7] which has implications for disease transmission.
Historically, Ae. aegypti were found in forested areas, using tree holes as aquatic habitats . As they have adapted to more urban domestic habitats, they have exploited a wide range of artificial containers such as vases, water tanks and tyres that are often associated with human habitations . They have also been found utilising underground aquatic habitats such as septic tanks  and adapting to use both indoor and outdoor aquatic habitats in the same area. Adaptation to breeding outdoors may allow for increased population numbers and difficulty in implementation of control methods . A study in Brazil found higher numbers of eggs in oviposition sites closer to human populations . Eggs are laid on or near the water surface  with the ability to survive desiccation .
Biting/resting habits (endo/exophily, endo/exophagy, biting periodicity)
The domestic form is often not found further than 100m from human habitations  although some studies have shown that breeding habitats can also be found away from human dwellings . Aedes aegypti prefer human habitations as they provide resting and host-seeking possibilities  and as a result will readily enter buildings [1, 5]. Their activity is both diurnal and crepuscular [5, 20].
Environmental thresholds/constraints/development criteria
Aedes aegypti, unlike Ae. albopictus is not able to undergo winter diapause as eggs, and this therefore limits their ability (to some extent) to exploit more northerly temperate regions (although some survival is possible during the summer following an importation). However it may establish in regions of Europe showing a humid subtropical climate (parts of Mediterranean and Black Sea countries) such as the Sochi region where it has become established again since 2001 (Black Seas coast).
Species competition has also been shown to affect distribution and abundance. A decrease in the distribution of Ae. aegypti has been associated with the invasion of Ae. albopictus, especially in south-eastern USA . They also have limited dispersal capability as adults  with a flight range estimate of only 200m .
Rainfall may affect abundance and productivity of breeding sites but this species’ preference for artificial water containers means it does not have to rely on rainfall for larval development sites . Coupled with its preference for feeding and resting indoors, these aspects make this species less susceptible to the effects of climatic factors which could influence its distribution.
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EPIDEMIOLOGY AND TRANSMISSION OF PATHOGENS
Known vector status (in field, experimental transmission)
Aedes aegypti is known to transmit dengue virus, yellow fever virus, chikungunya virus, and Zika virus. It is suggested to be a potential vector of Venezuelan Equine Encephalitis virus  and vector competency studies have shown Ae. aegypti is capable of transmitting West Nile virus. West Nile virus has also been isolated from this mosquito species in the field .
Role as enzootic or bridge vector
Yellow fever is maintained in nature between monkeys and mosquitoes [18, 25]. Aedes aegypti have been shown to transmit yellow fever virus to F1 progeny under laboratory conditions  and field collection studies have also confirmed this in nature .
Yellow fever virus can cause systemic disease including fever, jaundice, haemorrhage and renal failure. Symptoms are present in about one in seven of those infected  and the mortality rate is 20–50%.
Potential/Confirmed disease risk
Roughly three million tourists travel to yellow fever endemic areas from North America, Europe and Asia every year . Imported cases have been recently reported in Germany , Belgium , Spain, France, the Netherlands and Switzerland .
Role as enzootic or bridge vector
Aedes aegypti is the primary vector of dengue . All four dengue serotypes have been isolated from field-collected Ae. aegypti . Vertical transmission of dengue virus types 2,3 and 4 has been demonstrated  and although some suggest this is inefficient , others suggest that it plays a significant role in viral maintenance. In 2012, a large outbreak of dengue fever occurred in the Portuguese Autonomous Region of Madeira . The epidemic started in October 2012 and by early January 2013 more than 2 000 cases of dengue fever had been reported, with an additional 78 cases reported among European travellers returning from the island .
Dengue is prevalent in over 120 countries and is the most important mosquito borne disease affecting humans after malaria . It is a mosquito-borne viral disease caused by four serotypes which can cause intense fever headache, muscular and joint pain, anorexia, nausea, vomiting and rashes and sometimes severe disease with haemorrhages and shock syndrome. Dengue haemorrhagic fever and dengue shock syndrome can also occur and case fatality rates can reach 50% in untreated cases . There is currently no vaccine available against dengue but some promising trials were started during 2009 .
Potential/Confirmed disease risk
Aedes aegypti has long been recognised as a vector of dengue, causing major dengue fever epidemics in the Americas and South East Asia, where the incidence of the more severe form (dengue haemorrhagic fever) has been increasing . Global incidence of dengue has also increased in the past 25 years . Historically, outbreaks have also been reported in Europe, with one of the largest outbreaks on record occurring in Athens and neighbouring areas of Greece in 1927–1928 .
Role as enzootic or bridge vector
Aedes aegypti is the principle vector of chikungunya virus . Transovarial transmission was demonstrated by Aitken et al.  under laboratory conditions and the virus has been detected in wild-caught male Ae. aegypti  which may help with the maintenance of the virus in nature . Venereal transmission during mating has also been demonstrated under laboratory conditions, although it is thought to be lower than transovarial transmission .
Chikungunya infection can cause fever, myalgia, rash and arthraligia which can often last for months in up to 65% of patients . Clinical manifestations observed during an epidemic on Reunion Island included severe hepatitis, severe maternal and foetal disease and meningeoencephalitis . There is currently no licensed vaccine against chikungunya  but a recent study had success using virus-like particles to protect monkeys from high doses of chikungunya virus, the antibodies of which then protected immunodeficient mice against lethal doses of the virus .
Potential/Confirmed disease risk
Aedes aegypti have been involved in virtually all chikungunya epidemics from Africa, India and other countries in Southeast Asia . They caused an outbreak of chikungunya virus in Kenya (2004) and the Comoros islands (2005) where in the latter, 63% of the population were affected . A recent entomological investigation following an outbreak of chikungunya virus in Yemen (2010/2011) revealed the presence of chikungunya virus in field collected Ae. aegypti in the outbreak area. This represents the first isolation of chikungunya virus from field collected Ae. aegypti in Yemen .
Role as enzootic or bridge vector
Aedes aegypti has more recently been suggested as a vector of Zika virus which has been isolated from field-collected Ae. aegypti . This mosquito species has been shown to transmit the virus under laboratory conditions [43, 44]. Monkeys are suggested to be involved in transmission cycles of Zika virus. Antibodies to the virus have also been found in rodents .
Zika virus can cause headache, rash, malaise and back pain .
Potential/Confirmed disease risk
Zika virus is considered to be an emerging pathogen. An outbreak of Zika virus was reported in 2007 on Yap Island where 185 confirmed or suspected cases were reported. This was the first time the virus had been reported outside its usual geographical range, as previous cases had only been reported from Africa and Asia . Another outbreak in the Pacific was reported in French Polynesia in 2013 and later spread to New Caledonia .
Factors driving/impacting on transmission cycles
Distribution of dengue outbreaks is related to the simultaneous occurrence of its vectors, circulating virus and the availability of aquatic habitats. The spread of dengue has been aided by the global spread of Ae. aegypti over the past 25 years . Although currently limited in spread due to its intolerance to temperate winters, climate change could result in an increased distribution of Ae. aegypti.
As human population growth occurs in the future, sites in which this mosquito thrives will increase, providing further habitats for establishment. This coupled with the close proximity of humans and the tendency of Ae. aegypti to feed on multiple hosts during one gonotrophic cycle [5, 7], increases the risk of disease transmission in such areas. The movement of viraemic hosts can result in outbreaks from a number of arboviruses in non-endemic areas. It is estimated that 22.5 million passengers come to Europe each year and 185 000 of these could be viraemic for chikungunya alone .
The re-establishment of Ae. aegypti in some areas has resulted in disease transmission. Inadequate control of this invasive species could lead to its re-establishment in Europe which is why surveillance and research on this mosquito is so important.
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Public health (control/interventions)
The European Network on Imported Infectious Disease Surveillance was founded in 1999 and since then has noted an increase in imported cases of dengue into Europe. Two imported cases in the UK were fatal . Disease surveillance and reports of nuisance biting can be useful in identifying newly invaded areas. Over the past five years, 12 countries in Europe have set up surveillance for Ae. albopictus and other exotic mosquito species including Ae. aegypti  as they are often found in the same habitats. This number has increased to at least 14 after the rapid spread of Ae. albopictus in Italy and surveillance in the Netherlands has led to the identification of Ae. aegypti in tyres there.
Appropriate sampling strategy (aquatic immature stages sampling, adult trapping)
Human landing catches were successful for sampling Ae. aegypti during entomological surveying during an outbreak of yellow fever virus in Senegal . Ovitraps, bamboo and aspirators were used to collect eggs, larvae and adults during a study in Brazil . Modified ovitraps can also be used to collect gravid females by incorporating a sticky surface for the female to land on or residual insecticide to kill the female . Larval and pupae sampling using a dipper can also be useful, the latter for estimating adult population numbers . Another study in Brazil used ovitraps and MosquiTraps (modified ovitraps with the use of an attractant), the latter able to collect the eggs and the ovipositing female but also attracts species other than Ae. aegypti. The MosquiTraps are suggested to be more useful for assessing transmission risk as they can be used to measure direct proportions of populations involved in transmission . A limitation of using ovitraps as a method of control is that they need to be able to compete with existing oviposition sites within the environment. Mackay et al.,  provides evidence that increasing the size of the trap entrance and the surface area of water can improve trap efficacy.
Species specific control methods e.g. insecticide, public health education, etc
This mosquito species thrives in urban environments which provide it with numerous oviposition sites to lay eggs. Therefore, the distribution of this species is largely driven by human activities (e.g. storage of water outside) so control methods need to be directed at these factors . This is challenging because of the numerous sites in which Ae. aegypti lay eggs and in an urban setting, such sites are hard to access. A study in Mexico used a combination of quadrat and transect sampling methods to identify the most important containers for pupal development within 600 houses. They found an association between Ae. aepypti pupae and large cement washbasins. Targeted treatment of such sites could source reduction and the use of insecticides may be more successful in reducing mosquito numbers .
Historically, outbreaks of dengue and yellow fever have previously been controlled by Ae. aegypti eradication programmes but these have not always been successful and have resulted in the re-emergence of the diseases associated with this mosquito . In the 20th century, many eradication programmes were targeted at larval development sites in an attempt to eliminate yellow fever transmission and the use of DDT after the Second World War resulted in the eradication of the species from 22 countries in the Americas . This effort was discontinued and Ae. aegypti quickly re-colonised nearly all of the neotropics and subtropics . The use of insecticidal sprays have become less efficient since Ae. aegypti have become less accessible due to their time spent indoors . Eradication programmes set up in the 1950–60s (initiated by Pan American Health Organisation) in the Americas saw the reduction and eradication of Ae. aegypti there, but relaxation of mosquito management after the 1970s resulted in the re-establishment of Ae. aegypti, followed by dengue fever and DHF outbreaks .
Some other methods used include the introduction of predators into the larval habitats of Ae. aegypti e.g. copepods, the introduction of irradiated or genetically-modified mosquitoes (sterile male release) and the use of Wolbachia bacteria which can inhibit the replication of dengue virus within Ae. aegypti which could suppress or eliminate dengue transmission . Protective clothing and repellents are also advocated to reduce exposure to Ae. aegypti, along with indoor living spaces sprayed with pyrethrin . Sterile insect technique is another method that is being piloted for Ae. aegypti control during disease outbreaks e.g. dengue. Field studies in Malaysia show that engineered ‘genetically sterile‘ males had similar longevity as wild laboratory strains and that dispersal in the field was adequate .
Mosquito control programmes are suggested to be more effective against Ae. aegypti (as opposed to Ae. albopictus) due to its strong urban preference and strong human feeding preference . Using a combination of control methods as opposed to one single strategy is suggested to be most effective, and will reduce the chance of introducing selective pressures . However, using a combined control strategy of spraying insecticides, reducing potential breeding sites and increasing public health awareness in Madeira following the discovery of Ae. aegypti, did not stop this species re-establishing here .
Existing public health awareness and education materials
ECDC provides information on dengue, chikungunya, yellow fever and Zika virus which can be found at:
Many documents have been published in French overseas territories (Martinique in particular).
CDC also provide information on dengue, chikungunya and yellow fever which can be found at:
KEY AREAS OF UNCERTAINTY
It is clear that if Ae. aegypti re-establishes and spreads to its former regions in Europe it will have a significant impact on public health. The spread of Ae. aegypti needs to be monitored as this species is the primary vector of dengue, chikungunya and yellow fever viruses.
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