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Susceptibility of Ochlerotatus Taeniorhynchus and Culex Nigripalpus for Everglades Virus

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Susceptibility of Ochlerotatus Taeniorhynchus and Culex Nigripalpus for Everglades Virus Am. J. Trop. Med. Hyg., 73(1), 2005, pp. 11–16 Copyright © 2005 by The American Society of Tropical Medicine and Hygiene SUSCEPTIBILITY OF OCHLEROTATUS TAENIORHYNCHUS AND CULEX NIGRIPALPUS FOR EVERGLADES VIRUS LARK L. COFFEY* AND SCOTT C. WEAVER Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas Abstract. Everglades virus (EVEV), an alphavirus in the Venezuelan equine encephalitis (VEE) complex, is a mosquito-borne human pathogen endemic to South Florida. Field isolations of EVEV from Culex (Melanoconion) cedecei and laboratory susceptibility experiments established this species as its primary vector. However, isolates of EVEV from Ochlerotatus taeniorhynchus and Culex nigripalpus, more abundant and widespread species in South Florida, suggested that they also transmit EVEV and could infect many people. We performed susceptibility experi- ments with F1 generation Oc. taeniorhynchus and Cx. nigripalpus to evaluate their permissiveness to EVEV infection. In contrast to the high degree of susceptibility of Cx.(Mel.) cedecei, Oc. taeniorhynchus and Cx. nigripalpus were relatively refractory to oral EVEV infection, indicating that they are probably not important vectors. Identification of vectors involved in enzootic EVEV transmission will assist in understanding potential changes in vector use that could accompany the emergence of epizootic or epidemic EVEV. INTRODUCTION epidemics are believed to arise when mutations in enzootic subtype ID strains generate epizootic variants that produce Everglades virus (EVEV), a member of the Venezuelan high-titered viremias in horses, resulting in amplification and equine encephalitis (VEE) complex of alphaviruses (To- spillover to humans.11 EVEV, which generates only low-titer gaviridae: Alphavirus), is a human pathogen endemic to viremias in experimentally infected horses,12 may not be ca- South Florida that causes febrile illness and sometimes severe 1–3 pable of adapting for equine replication like the subtype ID neurologic disease. Everglades virus is transmitted among strains due to fundamental genetic differences. In other reservoir rodents by mosquito vectors (Figure 1) in the Ev- words, EVEV may be incapable of mutating to produce an erglades and surrounding regions of South Florida, in close 4,5 epizootic, equine amplification-competent phenotype. proximity to the Miami-Dade metropolitan area. This re- Limitations in vector infectivity and transmission potential gion is inhabited by more than 2 million people and hosts 6,7 could also explain the absence of EVEV emergence. Epi- more than 1 million visitors annually, suggesting the poten- zootic VEEV cycles involve several different mammalophilic tial for large-scale epidemic disease should EVEV emerge mosquito vectors,9,13 and adaptation to efficiently infect cer- like related VEE complex viruses. tain epizootic vectors such as Ochlerotatus taeniorhynchus VEE virus (VEEV) emergence depends on a combination may mediate efficient transmission to horses and people.14,15 of viral mutation, epidemiologic, and ecological events that EVEV may not efficiently infect vectors with the potential for must coincide in time and space. The close relationship of widespread epidemic transmission and/or may not have the EVEV to VEEV suggests that adaptation to equine amplifi- ability to readily adapt to these species. Further studies of cation hosts or mosquito vectors, as has been observed in EVEV-vector relationships could therefore improve under- VEEV epizootics and epidemics, could likewise mediate standing of the factors that limit EVEV transmission to hu- EVEV emergence. Although EVEV is similar in many re- mans and affect the potential for epidemic emergence and spects to other enzootic VEE complex viruses, there is no could assist in the development and implementation of strat- evidence that it has emerged to produce epidemics and egies to prevent potential disease. equine epizootics as have some other enzootic strains. De- Everglades virus vectors. Previous studies implicated Culex spite the lack of evidence of EVEV emergence, suggesting (Melanoconion) cedecei as the primary EVEV vector based that it does not pose a major public health risk, the recent on high infection rates in the field4 and its efficiency in trans- emergence of VEE in Mexico despite no previous history of mitting EVEV to naïve animals in laboratory experiments.16 subtype IE epizootics indicates that emergence potential of 8 Of the 7 vectors of enzootic VEE complex viruses identified VEE complex viruses is not entirely predictable. to date, all are members of the Spissipes section in the Culex The absence of EVEV emergence could be explained by (Melanoconion) subgenus.13 the lack of certain crucial ecological components of epizootic 9 Relatively little is known about the potential for mosqui- transmission in Florida. For example, the absence of large Cx. cedecei 10 toes other than to vector EVEV in the enzootic equine populations in South Florida may preclude efficient cycle. Although most studies of enzootic South and Central epizootic amplification. Extensive equine vaccination against American VEE complex virus ecology have incriminated a alphaviruses or natural, cross-protective immunity are other single Culex (Melanoconion) species as the principal vector at possibilities. a given locality, three different mosquito species were impli- Other possible explanations for the lack of EVEV emer- cated at a single forest in Colombia.17 Although evidence gence are related to the intrinsic amplification competence of supports the role of Cx. cedecei as the principal enzootic the virus and its potential for adaptation to new hosts. VEEV EVEV vector, numerous isolates of EVEV from other mos- quito species suggest that additional mosquitoes may also * Address correspondence to Lark L. Coffey, Department of Pathol- play a role in enzootic/endemic transmission. In field studies, ogy, University of Texas Medical Branch, 301 University Boulevard, 97 EVEV isolates were made from Ochlerotatus (previously Galveston, TX 77555-0609. E-mail: [email protected] Aedes) taeniorhynchus and 6 were made from Culex nigripal- 11 12 COFFEY AND WEAVER tively insusceptible to EVEV, as indicated by low levels of virus infectivity and dissemination after ingestion of relevant oral doses of virus, their extremely high densities in EVEV endemic areas could still allow for a considerable amount of human exposure to EVEV-infected mosquitoes. Several mar- ginally susceptible mosquito species have been implicated as VEEV vectors during epizootics when their large population sizes allow for transmission.13,29,30 As a related example, high densities of Aedes aegypti that were relatively resistant to infection with yellow fever virus were sufficient to initiate and maintain an urban epidemic in Nigeria.31 Alternatively, a lack of susceptibility of Oc. taeniorhynchus and Cx. nigripalpus may help explain the absence of recorded EVEV outbreaks. Therefore, we tested the susceptibility of these mosquitoes from South Florida to EVEV infection. MATERIALS AND METHODS FIGURE 1. Everglades virus transmission cycle. Arrows indicate cycling of Everglades virus via mosquito vectors and vertebrate res- Mosquito collection, identification, and rearing. Adult ervoir hosts. Organisms with an established role in the cycle are mosquitoes were collected in CDC light traps (John W. Hock highlighted in bold; those species postulated to participate are shown Company, Gainesville, FL) baited with dry ice in Mahogany in normal type. Hammock, Everglades National Park (ENP) (25°20Ј24Љ N, 080°49Ј22Љ W), Florida, in June 2003. Progeny derived di- rectly from natural populations were used to avoid changes in pus, and both species had minimum infection rates compa- susceptibility to virus infection that might result from coloni- rable to those of Cx. cedecei.4 Ochlerotatus taeniorhynchus zation and because Cx. nigripalpus mating is only successful has also been implicated as an important vector of epizootic/ under special circumstances in large outdoor cages.32 Mos- epidemic VEE complex viruses in South and Central quitoes were chilled and identified using morphologic crite- America.18–22 However, because the EVEV isolates made ria33 and were transported to an insectary at the University of from Oc. taeniorhynchus and Cx. nigripalpus may have been Texas Medical Branch, Galveston, Texas. Females of each present only in viremic blood-meals or in nondisseminated species were placed separately in 30 cm3 rearing cages at 27°C infections limited to the midgut, the potential for Oc. taenio- with a relative humidity of 80% and a 12 hour:12 hour (light: rhynchus and Cx. nigripalpus to serve as EVEV vectors re- dark) photoperiod. To detect natural infection with arbovi- mained to be tested using susceptibility experiments. ruses including EVEV, wild mosquitoes were offered blood Vector incrimination. Traditionally, incrimination of ar- meals from sentinel mice lacking functional interferon recep- thropods as vectors of viral pathogens involves four criteria: tors, which uniformly die when infected with most or all ar- 1) repeated demonstration of natural infection, 2) demonstra- boviruses endemic to South Florida including VEE complex tion of effective contact between the virus and vector, 3) es- viruses.34 Later, mosquitoes were supplied with hamster tablishment of a temporal and spatial association between the blood-meals at weekly intervals and 5% sucrose water
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