PUBLIC HEALTH IMPORTANCE OF THE INVASIVE MOSQUITOES OF EUROPE
Hansford K., Bennett E. & Medlock J.M., Medical Entomology group, Health Protection Agency, UK
3.1 Aedes albopictus
The invasive mosquito Aedes albopictus has recently been identified in Malta (Gatt et al., 2009; Buhagiar, 2009), adding another European country to the list of those now possibly at risk of the diseases this vector can transmit. Although the mosquito established itself in Europe for the first time in Albania in 1979 it has since been reported in 17 other European countries/micro-states, and has recently been recognised as a vector of disease in Europe.
Following the chikungunya virus (CHIKV) epidemics in the Indian Ocean (2005-2007), which caused millions of cases and significant morbidity and burden on health resources, the virus was imported into the first European country in 2007 and caused an autochthonously transmitted virus outbreak in Italy. This outbreak involved local transmission via Ae. albopictus mosquitoes and resulted in 205 cases (one fatal) with a further 129 suspected cases identified (Rezza et al., 2007). However, the true extent of this outbreak is said to be underestimated (Angelini et al., 2007). Imported cases of chikungunya have also been reported in Belgium, Czech Republic, France, Germany, Norway and United Kingdom, (Depoortere et al., 2006).
Aedes albopictus has also been associated with dengue virus (DENV) and has been implicated as the vector involved in the 1977-78 Seychelles (Metselaar D et al, 1980) and Reunion Island epidemics, an outbreak in Hawaii in 2001-2002 (Effer et al., 2005) and more recently in an outbreak in Reunion island again in 2004 and Mauritius in June 2009, which caused at least 220 cases (Pierre et al., 2005; Ramchurn et al., 2009). An estimated 50-100 million dengue cases occur annually worldwide (Paupy et al., 2009) and although dengue remains an imported infection in Europe, case numbers according to TropNetEurope are increasing: from 64 cases in 1999 to a maximum of 224 cases in 2002 and remaining at 100-170 cases since then (Jelinek, 2009). Data from INVS in France suggests that this number is higher, and since dengue was made notifiable in France in 2006, 420 imported cases were reported in 2007 alone. (Ledrans & Dejour Salamanca, 2010). Severe forms of dengue result in dengue haemorrhagic fever (DHF) and dengue shock syndrome, with case fatality rates reaching 50% in untreated cases (Seyler et al., 2009).
Aedes albopictus is also a known vector of Dirofilaria (filarial nematodes D. immitis and D. repens), a parasite transmitted primarily between dogs and mosquitoes, but which can also affect humans. Recent evidence has shown transmission of the parasite by Italian Ae. albopictus populations (Cancrini et al., 2003a; Cancrini et al., 2003b), coupled with an increase in prevalence of human dirofilariasis in Italy (Pampliglione et al., 2001).
A number of other viruses important to human health have been isolated from field collected Ae. albopictus in different countries and laboratory transmission of such viruses by Ae. albopictus has been demonstrated (Paupy et al., 2009). Such viruses include Eastern Equine encephalitis virus (Mitchell et al., 1992; Turell et al., 1994), La Crosse virus (Gerhardt et al., 2001; Grimstad et al., 1989), Venezuelan equine encephalitis virus (Beaman & Turell, 1991; Turell & Beaman, 1992), West Nile virus (WNV) (Holick et al., 2002: Sardelis et al., 2002c) and Japanese encephalitis virus (JEV) (Paupy et al., 2009). Field isolation and experimental infection studies alone do not mean this mosquito species is involved in transmission of these viruses, but the mosquito’s biting habits, increasing global distribution and recent involvement in a CHIKV outbreak highlights the importance of monitoring Ae. albopictus.
3.2 Aedes aegypti
Aedes aegypti is an invasive mosquito that has been found sporadically in Europe from Atlantic coast to the Black Sea (Christophers, 1960). It was supposed to be eradicated for decades, despite some occasional records from Italy in 1971 (Callot & Delécolle, 1972), and Turkey in 1984 and 2001 (B. Alten, pers. comm.), but new infestations have recently appeared in Madeira (Almeida et al., 2007) and southern Russia (A. Baranova, pers. comm.). Its establishment in more temperate zones is currently restricted due to its intolerance to temperate winters, but there is concern that this could change in the future should global climate change predictions become reality (Gould & Higgs, 2009).
Major dengue fever epidemics, due to Ae. aegypti, occur in the Americas, South East Asia and the western Pacific, and the disease is now endemic in >100 countries worldwide. Incidence of this disease has increased dramatically and the incidence of the more severe DHF has also been increasing (Wichmann & Jelinek, 2003). WHO estimates that there may be 50 million infections worldwide every year. This mosquito was once endemic in Europe and was responsible for large epidemics of dengue and yellow fever until its disappearance after the second world war; with the last dengue outbreak recorded in Greece in 1927-1928 (Rosen, 1986). Aedes aegypti is also known to cause outbreaks of CHIKV and has done so recently in Kenya, the Comoros, India, Mayotte (Gould & Higgs, 2009).
Additionally and importantly, Ae aegypti is a highly effective vector of yellow fever virus (YFV), a disease found in West, Central and East Africa (where large, severe epidemics have been recorded, with tens of thousands of deaths) and in South America. Imported yellow fever cases have been reported from Germany (Kiehl, 1999), Belgium (Colebunders, 2001), Spain, France, the Netherlands and Switzerland (Monath et al., 2002). Historically a YF outbreak occurred in Wales in the 19th century following importation of Ae. aegypti and infected passengers aboard a boat.
More recently, Ae. aegypti has been suggested as a vector of Zika virus (a flavivirus related to YFV, DENV, WNV, and JEV) owing to its isolation from field collections in Malaysia and in West Africa (Marchette et al., 1969, CRORA) and virus transmission under laboratory conditions (Boorman & Porterfield, 1956). The first outbreak of Zika virus, a relatively mild disease characterized by rash, arthralgia, and conjunctivitis, was reported in 2007 on Yap Island, Pacific Ocean, 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 (Hayes, 2009).
The re-establishment of this mosquito in Europe raises concerns about the autochthonous arbovirus transmission of pathogens such as DENV and CHIKV (Almeida et al., 2007), re-inforcing the need for surveillance of this mosquito species is Europe.
3.3 Aedes atropalpus
Aedes atropalpus is an invasive North American mosquito that has been found in Italy, (Romi et al., 1997), France (2003, S. Chouin & F. Schaffner unpublished data), and more recently in the Netherlands (Scholte et al., 2009). Although this latter introduction has shown little spread of the mosquito, preliminary modelling shows that climatic conditions in the Netherlands are not a limiting factor for further spread of this species here or in large parts of Europe (Scholte et al., 2009). Laboratory competency studies have shown the ability of Ae. atropalpus to transmit La Crosse virus (Freier & Beier, 1984), WNV (Turell et al., 2001) and other arboviral encephalitides, but its importance as a vector of infectious diseases is still not known (Scholte et al., 2009).
3.4 Aedes japonicus
Aedes japonicus is native to Korea, Japan, Taiwan, southern China and Russia (Tanaka, 1979) and was first reported in the US in 1998 (Peyton, et al., 1998), New Zealand in 1993 (Laird et al., 1994), northern France in 2000 (Schaffner et al., 2003), Belgium in 2002 (Versteirt et al., 2009), Switzerland and Germany in 2008 (Schaffner et al., 2009). Field-collected Ae. japonicus has been found positive for WNV on a number of occasions in the US (Andreadis et al., 2001) and laboratory studies show it is a competent vector of WNV (Sardelis & Turell, 2001; Turell et al., 2001). Laboratory studies have also shown Ae. japonicus to be a competent carrier of JEV (Takashima & Rosen, 1989), La Crosse virus (Sardelis et al., 2002b) and a moderately efficient vector for Eastern equine encephalitis (Sardelis et al., 2002a) and St Louis encephalitis virus (Sardelis et al., 2003). However, its role in the transmission of these viruses in natural conditions is unclear (Versteirt et al., 2009).
3.5 Aedes triseriatus
Aedes triseriatus is not yet known as established in Europe but it has been intercepted in a batch of used tyres imported from Louisiana (USA) to France, in 2004 (S. Chouin & F. Schaffner, unpublished data). Its ability to overwinter as diapausing eggs renders this species at risk for an establishment in Europe if repeated introductions. Found in the eastern half of the US in hardwood forests areas, Ae. triseriatus breeds in tree-holes, tyres and other artificial containers (Borucki et al., 2002). It is primarily zoophilic but is also known to bite humans (Freier & Grimstad, 1983). Aedes triseriatus is a known vector of La Crosse virus, first isolated from a fatal case in Wisconsin in 1960 and subsequently isolated in the field (Pantuwatana et al., 1972; Thompson et al., 1972; Watts et al., 1974). Transovarial transmission and vector competency have been demonstrated for this virus under laboratory conditions (Watts et al., 1973). La Crosse virus can cause serious disease in humans and is the most common cause of paediatric arboviral encephalitis in the US with 42-172 cases reported annually (Borucki et al., 2002). Case numbers, however, are suspected to be underestimated (McJunkin et al., 2001).
Jamestown canyon virus has repeatedly been isolated from field-collected Ae. triseriatus in the US (Andreadis et al., 2008) and the mosquito has also been suggested to be a possible bridge vector for WNV following isolations of the virus from field collections (CDC, 2009) and vector competence studies under laboratory conditions (Styler et al., 2007). Other vector competence studies have shown its ability to transmit Venezuelan equine encephalitis (Davis et al., 1966), Eastern equine encephalitis, Western equine encephalitis, Dengue (type I), St Louis encephalitis virus and YFV under laboratory conditions (Freier & Grimstad, 1983).
Almeida, A.P.G., Goncalves, Y.M., Novo, M.T., Sousa, C.A., Melim, M. & Gracio, A.J.S. (2007)Vector monitoring of Aedes aegypti in the Autonomous Region of Madeira, Portugal. Eurosurveillance12(46) avail online
Andreadis, J.F., Anderson, , J.F., Munstermann, L.E., Wolfe, R.J. & Florin, D.A. (2001) Discovery, distribution and abundance of the newly introduced mosquito Och japonicus in Connecticut, USA. Journal of Medical Entomology 38(6) pp774-749
Andreadis, T.G., Anderson, J.F., Armstrong, P.M. & Main, A.J. (2008) Isolations of Jamestown Canyon virus from field collected mosquitoes in Connecticut, USA: a ten year analysis, 1997-2006. Vector Borne Zoonotic Diseasese 8(2) pp175-188
Angelini, R., Finarelli, A.C., Angelini, P., Po, C., Petropulacos, K., Silvi, G., Macini, P., Fortuna, C., Venturi, G., Magurano, F., Fiorentini, C., Marchi, A., Benedetti, E., Bucci, P., Boros, S., Romi, R., Majori, G., Ciufolini, M.G., Nicoletti, L., Rezza, G. & Cassone, A. (2007) Chikungunya in north-eastern Italy: a summing up of the outbreak. Eurosurveillance 12(47) Beaman, J.R. & Turell, M.J. (1991)
Transmission of Venezuelan equine encephalomyelitis virus by strains of Aedes albopictus (Diptera: Culicidae) collected in North and South America Journal of Medical Entomology 28(1) pp161-164
Boorman, J.P.T. & Porterfield, J.S. (1956) A simple technique for infection of mosquitoes with viruses transmission of zika virus. Transactions of the Royal Society of Tropical Medicine and Hygiene 50(3) pp238-242
Borucki, M.K., Kempf, B.J., Blitvich, B.J.,Blair, C.D. & Beaty, B.J. (2002) La Crosse virus: replication in vertebrate and invertebrate hosts Microbes and Infection 4 pp341-350
Buhagiar, J.A. (2009) A second record of Aedes (Stegomyia) albopictus (Diptera: Culicidae) in Malta. European Mosquito Bulletin 27 pp65-67
Callot, J. & Delécolle, J.C. (1972) Notes d'entomologie – VI. Localisation septentrionale d'Aedes aegypti. Ann. Parasitol. 47 pp665
Cancrini, G., Frangipane di Regalbono, A., Ricci, I., Tessarin, C., Grabrielli, S. & Pietrobelli, M. (2003a) Aedes albopictus is a natural vector of Dirofilaria immitis in Italy. Veterinary Parasitology, 118(3-4) pp195-202
Cancrini, G., Romi, R., Gabrielli, S., Toma, L., Paolo, M., diScaramozzino, P., (2003b). First finding of Dirofilaria repens in a natural population of Aedes albopictus. Med. Vet. Entomol. 17(4) pp448–451
CDC (2009) Mosquito Species producing WNV positives by year
Christophers, S. (1960) Aëdes aegypti (L.). The yellow fever mosquito. Its life history, bionomics and structure. University Press, Cambridge, UK.
Colebunders, R. (2001) Imported case of confirmed yellow fever detected in Belgium Eurosurveillance 5(45)
Davis, M.H., Hogge, A.L., Corristan, E.C. & Ferrell, J.K. (1966) Mosquito transmission of Venezuelan equine encephalomyelitis virus from experimentally infected dogs American Journal of Tropical Medicine and Hygiene 15(2) pp227-230
Depoortere, E. & Coulombier, D. (2006) Chikungunya risk assessment for Europe: recommendations for action. Eurosurveillance 11(19)
Effer, P.V., Pang, L., Kitsutani, P., Vorndam, V., Nakata, M., Ayers, T., Elm, J., Tom, T., Reiter, P., Rigau-Perez, J.G., Hayes, J.M., Mills, K., Napier, M., Clark, G.G. & Gubler, D.J. (2005) Dengue fever, Hawaii, 2001-2002. Emerging Infectious Diseases 11 pp742-749
Freier, J.E. & Beier, J.C. (1984) Oral transmission of La Crosse virus by Aedes atropalpus. American Journal of Tropical Medicine and Hygiene 33(4) pp708-714
Freier, J.E. & Grimstad, P.R. (1983) Transmission of dengue virus by orally infected Aedes triseriatus. American Journal of Tropical Medicine and Hygiene 3(6) pp1429-1434
Gatt, P., Deeming, J.C. & Schaffner, F. (2009) First records of Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae) in Malta European Mosquito Bulletin 27 pp56-64
Gerhardt, R.R., Gottfried, K.L., Apperson, C.S., Davis, B.S., Erwin, P.C., Smith, B, Panella, N.A., Powell, E.E. & Nasci, R.S. (2001) First isolation of La Crosse virus from naturally infected Aedes albopictus. Emerging Infectious Diseases 7(5) pp807-811
Gould, E.A. & Higgs, S. (2009) Impact of climate change and other farctors on emerging arbovirus diseasesTransactions of the Royal Society of Tropical Medicine and Hygiene 130(2) pp109-121
Grimstad, P.R., Kobayashi, J.F., Zhang, M.B. & Craig G.B. (1989) Recently introduced Aedes albopictus in the United States: potential vector of La Crosse virus (Bunyaviridae: California serogroup). J Am Mosq Control Assoc. 5(3) pp422-427
Hayes, E.B. (2009) Zika virus outside Africa Emerging Infectious Diseases 15(9) pp1347-1350
Holick, J., Kyle, A., Ferraro, W., Delaney, R.R. & Iwaseczko, M. (2002) Discovery of Aedes albopictus infected with west nile virus in southeastern Pennsylvania. J Am Mosq Control Assoc. 18(2) pp131
Ledrans, M. & Dejour Salamanca D. (2008) Cas importés de chikungunya et de dengue en France métropolitaine Institut de veille sanitaire, Saint-Maurice, pp28
Jelinek, T. (2009) Trends in the epidemiology of dengue fever and their relevance for importation to Europe. Euro Surveil 14(25)
Kiehl, W. (1999) Suspected case of haemorrhagic fever confirmed as yellow fever in Germany. Euro Surveil. 3(33)
Laird, M., Calder, L., Thornton, R.C., Syme, R., Holder, P.W. & Mogi, M. (1994) Japanese Aedes albopictus among four mosquito species reaching New Zealand in used tires. J Am Mosq Control Assoc. 10(1) pp14-23
McJunkin, J.E., De Los Reyes, E.C., Irazuzta, J.E., Caceres, M.J., Khan, R.R., Minnich, L.L., Fu, K.D., Lovett, G.D., Tsai, T. & Thompson, A. (2001) La Crosse encephalitis in children.The New England Journal of Medicine 3(11) pp801-807
Marchette, N.J., Garcia, R. & Rudnick, A. (1969) Isolation of zika virus from Aedes aegypti mosquitoes in Malaysia. The American Journal of Tropical Medicine and Hygiene 18(3) pp411-415
Metselaar D, Grainger CR, Oei KG, Reynolds DG, Pudney M, Leake CJ, Tukei PM, D'Offay RM, Simpson DI. (1980) An outbreak of type 2 dengue fever in the Seychelles, probably transmitted by Aedes albopictus (Skuse). Bull World Health Organ. 58(6):pp 937-943
Mitchell, C.J., Niebylski, M.L., Smith, G.C., Karabatsos, N., Martin, D., Mutebi, J.P., Craig, G.B. & Mahler, M.J. (1992) Isolation of eastern equine encephalitis virus from Aedes albopictus in Florida. Science 257(5069) pp526-527
Monath, T.P. & Cetron, M.S. (2002) Prevention of Yellow Fever in Persons Traveling to the Tropics. Clinical Infectious Diseases 34(10) pp1369-1378
Pampiglione, S., Rivasi, F., Angeli, G. & Boldorini, R. (2001) Dirofilariasis due to Dirofilaria repens in Italy, an emergent zoonosis: Report of 60 new cases. Histopathology 38 pp344-354
Paupy, C., Delatte, H., Bagny, L., Corbel, V. & Fontenille, D. (2009) Aedes albopictus, an arbovirus vector: From the darkness to the light. Microbes and Infections 11(14-15) pp1177-1185
Peyton, E.L., Campbell, S.R., Candeletti, T.M., Romanowski, M. & Cran, W.J. (1999) Aedes j japonicus, a new introduction into the United States. Journal of the American Mosquito Control Association 15(2) pp238-241
Pierre, V., Thiria, J., Rachou, E., Sissoko, D., Lassalle, C. & Renault, P. (2005) Epidémie de dengue 1 à la Réunion en 2004. Journées de veille sanitaire, Paris, Abstract bookpp64,
Puntuwatana, S., Thompson, W.H., Watts, D.M. & Hanson, R.P. (1972) Experimental infection of chipmunks and squirrels with La Crosse and Trivittatus viruses and biological transmission of La Crosse by Aedes triseriatus. American Journal of Tropical Medicine and Hygiene 21(4) pp476-81
Ramchurn, S.K., Moheeput, K. & Goorah, S.S. (2009) An analysis of a short-lived outbreak of dengue fever in Mauritius. Eurosurveillance 14(34)
Rezza, G., Nicoletti, L., Angelini, R., Romi, R., Finarelli, A.C., Panning, M., Cordiolo, P., Fortuna, C., Boros, S., Magurano, F., Silvi, G., Angelini, P., Dottori, M., Ciufolini, M.G., Majori, G.C. & Cassone, A. (2007) Infection with CHIKV in Italy: an outbreak in a temperate region. The Lancet 370(9602) pp1840-1846
Romi, R., Sabtinelli, G., Savelli, L.G., Raris, M., Zago, M. & Malatesta, R. (1997) Identification of a North American mosquito species Aedes atropalpus in Italy.J Am Mosq Control Assoc. 13(3) pp245-246
Rosen, L. (1986) Dengue in Greece in 1927 and 1928 and the pathogenesis of DHF: new data and a different conclusion. The American Society of Tropical Medicine and Hygiene 35(3) pp642-653
Sardelis, M.R. & Turell, M.J. (2001) Oc j japonicus in Frederick County, Maryland: discovery, distribution and vector competence for West Nile virus. Journal of the American Mosquito Control Association 17(2) pp137-141
Sardelis, M.R., Dohm, D.J., Pagac, B., Andre, R.G. & Turell, M.J. (2002b) Experimental transmission of eastern equine encephalitis virus by Oc j japonicus.Journal of Medical Entomology 39(3) pp480-484
Sardelis, M.R., Turell, M.J. & Andre, R.G (2002a) Laboratory transmission of La Crosse virus by Oc j japonicus. Journal of Medical Entomology 39(4) pp635-639
Sardelis, M.R., Turell, M.J., O'Guinn, M.L., Andre, R.G. & Roberts, D.R. (2002c) Vector competence of three North American strains of Aedes albopictus for West Nile virus. J Am Mosq Control Assoc. 18(4) pp284-289
Sardelis, M.R., Turell, M.J. & Andre, R.G. (2003) Experimental transmission of St Louis encephalitis virus by Oc j japonicus. Journal of the American Mosquito Control Association 19(2) pp159-162
Schaffner, F., Chouin, S. & Guilloteau, J. (2003) First record of Ochlerotatus japonicus in metropolitan France. Journal of the American Mosquito Control Association 19(1) pp1-5
Schaffner F, Kaufmann C, Hegglin D & Mathis A (2009) The invasive mosquito Aedes japonicus in central Europe. Medical & Veterinary Entomology 23 (4): 448-451
Scholte, E.J., Hartog, W.D., Braks, M., Reusken, C., Dik, M. & Hessels, A. (2009) First report of a North American invasive mosquito species Ochlerotatus atropalpus in the Netherlands, 2009 Eurosurveillance 14(55) avail online:
Seyler, T., Grandesso, F., Strat, Y.L., Tarantola, A. & Depoortere, E. (2009) Assessing the risk of importing dengue and chikungunya viruses to the European Union. Epidemics 1(3) pp175-184
Styler, L.M., Kent, K.A., Albright, R.G., Bennett, C.J., Kramer, L.D. & Bernard, K.A. (2007) Mosquitoes inoculate high doses of West Nile Virus as they probe and feed on live hosts. PLoS Pathogens 3(9) e132 doi:10.1371/journal.ppat.0030132
Takashima, I. & Rosen, L. (1989) Horizontal and vertical transmission of Japanese encephalitis virus by Aedes japonicus. Journal of Medical Entomology 26 pp454-458
Tanaka, K. (1979) A revision of the adult and larval mosquitoes of Japan (including the Ryukyu Archipelago and the Ogasawara islands) and Korea. Contributions of the American Entomological Institute 16 pp1-987
Thompson, W.H., Anslow, R.O., Hanson, R.P. & Defoliart, G.R. (1972) La Crosse isolations from mosquitoes in Wisconsin 1967-1968. American Journal of Tropical Medicine and Hygiene 21(1) pp90-96
Turell, M.J. & Beaman, J.R. (1992) Experimental transmission of Venezuelan equine encephalomyelitis virus by a strain of Aedes albopictus (Diptera: Culicidae) from New Orleans, Louisiana. J. Med. Entomol. 29(5) pp802-805
Turell, M.J., Beaman, J.R. & Neely, G.W. (1994) Experimenatl transmission of eastern equine encephalitis virus by strains of Aedes albopictus and A. taeniorhynchus (Diptera: Culicidae). J. Med. Entomol. 31(2) pp287-290
Turell, M.J., O’Guinn, M.L., Dohm, D.J. & Jones, J.W. (2001) Vector competence of North American mosquitoes for West Nile virus. Journal of Medical Entomology 38(2) pp130-134
Versteirt, V., Schaffner, F., Garros, C., Dekoninck, W., Coosemans, M. & Bortel, W. (2009) Introduction and establishment of the exotic mosquito species Aedes j japonicus in Belguim. J. Med. Entomol. 46(6) pp1464-1467
Watts, D.M., Pantuwatana, S., DeFoliart, G.R., Yuill, T.M. &Thompson, W.H. (1973) Transovarial transmission of La Crosse virus in the mosquito Aedes triseriatus. Science 182(117) pp1140-1141
Watts, D.M., Thompson, W.H., Yuill, T.M., Defoliart, G.R. & Hanson, R.P. (1974) Overwintering of La Crosse virus in Aedes triseriatus. American Journal of Tropical Medicine and Hygiene 23(4) pp694-700
Weaver, S.C. & Reisen, W.K. (2009) Present and future arboviral threats. Antiviral Research (Epub ahead of print)
Wichmann, O. & Jelinek, T. (2003) Surveillance of imported dengue infections in Europe Euro Surveil7(32)