Spatial-temporal analysis of Cache Valley virus (Bunyaviridae: Orthobunyavirus) infection in anopheline and culicine mosquitoes (Diptera: Culicidae) in the northeastern United States, 1997-2012

Abstract

Cache Valley virus (CVV) is a mosquito-borne bunyavirus (family Bunyaviridae, genus Orthobunyavirus) that is enzootic throughout much of North and Central America. White-tailed deer (Odocoileus virginianus) have been incriminated as important reservoir and amplification hosts. CVV has been found in a diverse array of mosquito species, but the principal vectors are unknown. A 16-year study was undertaken to identify the primary mosquito vectors in Connecticut, quantify seasonal prevalence rates of infection, and define the spatial geographic distribution of CVV in the state as a function of land use and white-tailed deer populations, which have increased substantially over this period. CVV was isolated from 16 mosquito species in seven genera, almost all of which were multivoltine and mammalophilic. Anopheles (An.) punctipennis was incriminated as the most consistent and likely vector in this region on the basis of yearly isolation frequencies and the spatial geographic distribution of infected mosquitoes. Other species exhibiting frequent temporal and moderate spatial geographic patterns of virus isolation within the state included Ochlerotatus (Oc.) trivittatus, Oc. canadensis, Aedes (Ae.) vexans, and Ae. cinereus. New isolation records for CVV were established for An. walkeri, Culiseta melanura, and Oc. cantator. Other species from which CVV was isolated included An. quadrimaculatus, Coquillettidia perturbans, Culex salinarius, Oc. japonicus, Oc. sollicitans, Oc. taeniorhynchus, Oc. triseriatus, and Psorophora ferox. Mosquitoes infected with CVV were equally distributed throughout urban, suburban, and rural locales, and infection rates were not directly associated with the localized abundance of white-tailed deer, possibly due to their saturation throughout the region. Virus activity in mosquitoes was episodic with no consistent pattern from year-to-year, and fluctuations in yearly seasonal infection rates did not appear to be directly impacted by overall mosquito abundance. Virus infection in mosquitoes occurred late in the season that mostly extended from mid-August through September, when adult mosquito populations were visibly declining and were comparatively low. Findings argue for a limited role for vertical transmission for the perpetuation of CVV as occurs with other related bunyaviruses.

Keywords: Anopheles punctipennis; Bunyaviridae; Cache Valley virus; Mosquito; Orthobunyavirus.

FIG. 1.

Land use map of Connecticut showing white-tailed deer management zones (1–12), geographic distribution of mosquito collection sites, and Cache Valley virus (CVV) isolations obtained from mosquitoes collected from 1997 to 2012.

FIG. 2.

Cluster graph depicting the distribution and prevalence of Cache Valley virus (CVV) isolations among 16 species of mosquitoes as a function of (1) total number of virus isolations, (2) number of years virus was detected, and (3) number of sites virus was isolated from for in each species.

FIG. 3.

Relationship between estimated white-tailed deer populations in 10 deer management zones in Connecticut and calculated Cache Valley virus (CVV) maximum likelihood estimations (MLEs) from mosquitoes trapped in those zones from 1997 to 2012. Numbers correspond to specific deer management zone shown in Figure 1.

FIG. 4.

Yearly number of Cache Valley virus (CVV) isolations from mosquitoes and overall bias corrected minimum field infection rates (maximum likelihood estimation [MLE]) in relation to number of mosquitoes trapped and tested 1997 to 2012.

FIG. 5.

Weekly isolations and bias corrected minimum field infection rates (MLE) of Cache Valley virus (CVV) from field-collected mosquitoes in Connecticut in relation to overall mosquito abundance, 1997 to 2012.

FIG. 6.

Weekly summaries of Cache Valley virus (CVV) isolations from 16 mosquito species in relation to mosquito abundance, 1997 to 2012. (•) CVV detected; (○) CVV not detected.