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424 JounNar,oF THEAurnrcex Mosqurro CoNrnor Assocrenon Vor, 2, No. 4

AEDESAI^BOPICTUS AND : A CONCISEREVIEW OF THE LITERATUREI,2

DONALD A. SHROYER Florida Laboratory, Institute of Food and Agricultural Sciences,University of Florida, 200 9th StreetS. E., Vero Beach,FL 32962

ABSTRACT. Aedesalbopichu is an efficient vector of the four dengue , and it is also capable of transovarially transmittind these viruses. Aetlesahobbnu can also serv:eas a host and/or vector of several additional aiboviruses, so"meof which are of considerable medical or veterinary importance. This review compiles previously published studiesthat have demonstrated an experimental or natuial associationbetween Ae. albopictusand specific arboviruses.

INTRODUCTION Unfortunately, it has sometimes been further assumed that Ae. aegyptiis an especially The recent establishment fficient of Aedcsalbopictr.ts vector of dengue viruses. This is not the case. (Skuse) in North America (Sprenger and A comprehensive study by Rosen et aI. 1986) Wuithiranyagool is a concern for at least (1985) compared the susceptibility of Ae. two reasons. Not only is it a formidable pest albopictru and Ae. aegJpti to oral infection with Ae. , but albopictusis a known or each of'the dengue viruses. In every case, a potential vector to man of several arboviruses. significantly larger proportion of the Ae. know much We about the vector competence albopictusbecame infected when both species of this speciesfor some viruses, but there are were fed on the same infected blood source. many important gaps in our knowledge. In this The relative efficiency of these species to review I have attempted to briefly summarize transmit dengue viruses by bite once they are what is known of the ability of Aedzsahopicttu infected has not been as well-studied. Surpris- to serve as a host and/or vector of arboviruses. ingly little has been published regarding the This report does zof constitute a comprehen- 'efficiencyof either Aa. aegyptior Ae. albopictusto sive review of all past studies that transmit dengue viruses by bite. For technical have involved Ae, albopictus,nor does it attempt reasonsit has been impossible until recently to to inform in depth. The intent is instead to reliably quantitate oral of dengue identify only those basic, published reports viruses by mosquitoes (Gubler and Rosen which demonstrate an experimental or natural 1976). Jumali et al. (1979) were able to associationbetween particular viruses and this simultaneouslycompare IndonesianA e. albopictru mosquito. Important, but as yet unpublished and, Ae. aegpti infected with dengue-3 , studies of Ae. albopictruwill not be discussedin and found that the species were equally this review. efficient in transmission by the oral route. The best early evidence that Ae. albopictu"scould DISCUSSION transmit dengue viruses came from studies of Simmons et al. (1930), in which human It is popular belief that Aadesaegypti (Linn.) is volunteers suffering from dengue were used to the sole vector of the four distinct viruses infect Ae. albopictu,sfemales that engorged upon which causethe specrum of diseasesymptoms them. These same Aa. albopictusmosquitoes that we collectively term "dengue" (including were then able to transmit dengue to other , dengue hemorrhagic fever and dengue shock syndrome). This belief is largely volunteers after a suitable period of incubation. due to the undisputed involvement of Ae. Aedcsalbopictus has been repeatedly incrimi- acgyptiin many large epidemics of this disease. nated as a vector during dengue outbreaks, However, other Aedes(Stegomyia) species are particularly in SoutheastAsia. Notablealbopichts- known dengue vectors,and may be responsible associated epidemics include those in for the occurrence of these viruses in locales (Sabin 1952), (Gould et al. 1968), where Ae. eeg)Qtiis absent (Rosen et al. 1985). Singapore (Chan et al. l97l), Central Java (Jumali et al. 1979), and the Republic of Seychelles(Metselaar et al. 1980). I University of Florida, Institute of Food and Aedcsalbopictu,s is also a potential vector of Agricultural Sciences,Experiment Station Journal several additional arboviruses. some of which SeriesNo. 7384. are of considerablemedical importance (Table 2 Presented at a symposium entided "Aedcsahopithu in the Americas" at the annual meeting of the l). For example, Ae. albopictu.scan be easily American Association,New Orleans, infected in the laboratory by ingestion of Louisianaon April 21, 1986. virus, which causesa dengue-like DncnMsrn.1986 Anoos ttaoptctus AND ARBoVIRUSES 425

Table l. Susceptibilityof Aedcsahopictlts to oral infection with arboviruses,and its ability to transmit them by bite.

Oral Oral Infected in Virus infection? transmission? nature? Referencesu

Chikungunya T T I Dengue(-1,-2,-3,-4) T + + 2-6 Japaneseencephalitis T + T 7-9 Nodamura + l0 Orungo + + ll RossRiver + + 12 San Angelo T - t3-15 St. Louis T f l6 West Nile T l7 Western equine T + l8 + + l9 "(l) MangiaficolgTl,(2)Chanetal.l97l,(3)Rosenetal.l985,(4)Rudnick1966,(5)Simmonsetal.l930, (6) Smith et-al. 1971,(7) Huang 1957,(8) Rosenet al. 1978,(9) Wu and Wu 1957,(10) Tesh 1980b,(ll) Tomori and Aitken 1978,(12) Kay et al. 1982,(13) Shroyer 1986,(14) Tesh 1980a,(15) Tesh and Shroyer 1980,(16) Mitamura et al. 1940,cited in Ferguson1954, (17) Akhter et al. 1982,(18) Simmons et al. 1936,(19) Dinger et al. 1929,cited in Warren 1951.

"transovarial diseasein man (Mangiafico 1971,Yaminishi et transmission."For at least some al. 1983). Aedcsalbopicttu infected by the oral arboviruses, it is clear that ransovarially route are also capable of efficient transmission transmitted virus is essential to the virus life of Chikungunya virus by bite (Mangiafico cycle,while vertebrate infections may be largely "dead-ends" 197l). incidental (DeFoliart 1983,Patrican Table I also shows that Ae. albopictusis et al. 1985). All four dengue viruses are capable of transmitting transovarially transmissible by Ae. albopictus virus by bite, and that this virus has reportedly (Rosen et al. 1983), as are the other viruses been isolated from field-collected mosquitoes shown in Table 2. Note that the list of (Huang 1957, Wu and Wu 1957).The latter transovarially transmissibleviruses includes St. observation suggests that Ae. albopicttu virus Louis and Japaneseencephalitis viruses, as well may serveas a vector ofJapanese encephalitis as three of the California encephalitis group in some areas, although it is not presently believed to be a major vector. Table 2. Arbovirusesthat canbe transovarially Laboratory studies have shown that Ae. transmittedby Aedesalbopittus. albopictusis susceptible to oral infection with the remaining viruseslisted in Table I and that Virus References" (with the exception of Nodamura virus) these Flauiairuses viruses can be transmitted by bite. In some Banzi I casesthe demonstrated susceptibilityand trans- Bussuquara 2 missibilityis only marginal. In other cases(eg., Dengue-l 3 ) it is clear that the vector Dengue-2 3 Dengue-3 3 of the speciesis very high. It is competence Dengue-4 3 noteworthy that Table I includes St. Louis Ilheus 9 encephalitis, yellow fever, West Nile, Ross Kokobera 2 River, Western equine encephalomyelitisand Kunjinb 2 Orungo viruses, which are all capable of Japaneseencephalitis 4 causing serious disease in man. Additional, St. Louis encephalitis I more extensivestudy of the potential of Aa. Uganda S I albopichuas a vector of these viruses is grgently Bunyaaintses needed to evaluate the significance of these Keystone 2 preliminary studies. La Crosse 2 Feeding on a viremic vertebrate is not the San Angelo 9 only method by which a mosquitocan become " (l) Tesh et al. 1979,(2) Tesh 1980a,(3) Rosenet infected with an arbovirus. Infected female al. 1983,(4) Rosenet al. 1978,(5) Hardy et al. 1980. mosquitoes can directly transfer arbovirus b Venereally transmissibleby infected males (Tesh infections to their offspring, a process called l98l). 426 Jounrter oF THEArr.rnnrceN Mosqurro Corqrnor AssocrarroN Vor,.2,No.4

viruses- (Table 2). We probably know more Table 3. Additional arbovirusesknown to replicate about the mechanism ofiransovarial transmis- following inocularion of Aed.csatbofuns. sion of arboviruses in Ae. ahopi.cttuthan in any other mosquito, yet we geneially have only a Virus Referencesa vague impression of the efficiency of transova- Alplnainues rial transmissionof any particulaf virus. This is Sindbis due to an incomplete understanding of the Phleboviruses conditions and factors which influince the Arumowat 2 proportion of Ae. albopictus females that Bujaru I transovarially transmit, and the -foundproportion of Chilibre I ransovarially infected offspring within Icoaraci 9 individual families. It is not piesently known Itaporanga 2 whether transovarialtransmission bv Ae.'atbobitats Karimabad I Pacui plays an important role in the natural hiitory 2 Salehabad 9 of any of theseviruses. Rlnbd,ovinues In the laboratory it is relatively easy'canto isolate families of Ae. albopicttu which very Chandipurab 3 Cocal efficiently transmit Sah Angelo virus (Califor- 4 Gray Lodgeb 3 nia encephalitis group) by the transovarial rou^te(Te_sh Joinjakakab 3 and Shroyer 1980, Shroyer 1986). Piryo In fact, 38 consecutive . 3 generations of transova- Sigmao 3 rial transmissionof San Angelo virus have been Vesicular stomatitis-NJb 3 monitored in Aedesalbopicttu (Shroyer 1986). These Unclassifud mosquitoes were neaer exposed to an Matsuo infected vertebrate, yet most mosquitoes were a infected. Essentially all females that are (l) Stollar and Hardy 1984, (2) Tesh l97b, (B) Rosen transovarially infectid with San Angelo virus 1980, (4) Hurlbut and Thomas 1969, (5) Rosenand Shroyer 1981. produce at least one infected offsdring, but o "moth- Induce lethal sensitivity to carbon dioxide. there is considerable variation betw-een ers in the _proportion of infected offspring ping distributions. Clearly, medical entomology produced. We need to know whethei thi does not deal with an unchanging world. mechanism of transovarial transmission of other America arboviruses in Ae. albopictruis similar to that of San Angelo virus. Finally, Aedzsalbopictu.s is capableof support- CONCLUSIONS ing growth of several arboviruses for which there is no information regarding their ability , I have tried to briefly convey some notion of to orally infect, or to be iransm-=ittedby bite the known and potential capacity of Ae. (Table 3). We know only that these viruses will albopicttu to serve ai arbovirus host and vector. replicate when injected into the body of Ae. It is clear that for some of these viruses. the albopitttu.Some of these viruses induce a lethal species could have the capacity to serve as a paralysis in Ae. alhopiclruwhich is expressed vector under appropriate environmental cir- only if the infected mosquito is exposed briefly cumstances. We know that Ae. albopichts is an to a high concentration of carbon dioxide gas excellent vector of dengue viruses. Yet there (Rosen 1980).The previously mentioned S-an are many unanswered questions that require Angelo virus also induces such carbon dioxide the urgent artention of ihe scientific commu- sensitivity(D. A. Shroyer,unpublished data). nity. We need ro know whether North Ameri- Aedcsalbopittns is not known to be a natural can populations of Aa. albofutu.s are sufficiently host of any of the viruses listed in Table 3, and susceptible ro infection wilh the other impor- there may be a tendency for such information tant American arboviruses and whether trans- to be regarded as having little relevance. mission by bite is efficient enough to permit the However, until 1985, the distribution of Ae. specles to serve as a natural vector. albopictru and San Angelo virus were not Should Ae. albopicttu spread into Central known to- o-verlap, San Angelo virus being America and the Caribbean, will the severity of known only from Texas, Arizona, New Mexico, dengue disease in these areas be affected? It and Colorado (Calisher 1983).Studies of San has been hypothesized that Ae. aegypti- Angel_ovirus in Ae. albopicttts,which previously transmitted dengue epidemics tend to result in served only as an experimental model, might more severe forms of disease, such as fatal now take on new significance with the discov- hemorrhagic fever (Rosen et al. 1985). It is ery that this virus and mosquito have overlap- thought that the relatively low susceptibility of DncnMsrn,1986 Anonsnnoptcrus AND Annovrnuses 427

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