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The association of winds with the spread of EHDV in dairy cattle in Israel during an outbreak in 2006

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Abstract

Winds may play a major role in spread of arthropod-borne viruses (arboviruses). Arboviruses like epizootic hemorrhagic disease virus (EHDV), bluetongue virus and bovine ephemeral fever virus (BEFV) frequently cause major outbreaks in Israel with a unique pattern of spread. Most of these outbreaks begin in the Jordan valley, near the Sea of Galilee and then spread to the north, south and west through the major valleys of Israel. The aim of this study was to describe the spread pattern in such an outbreak and to find if this pattern can be explained by winds. Herein, we compared the spread rate to each direction and used Cox proportional hazards model to test factors associated with the spread of EHDV, which emerged in diary cattle in Israel during the summer of 2006. Documented, clinical and serological data on spread of the outbreak were then compared with wind data collected by meteorological stations along the trail of virus spread and with modeled winds at high altitude (>500 m). The analysis revealed that both the hazard and the rate of outbreak spread to the south and to the north were significantly higher than to the west. Average rate of outbreak spread during periods in which at least 3 h of winds to spread direction were recorded was 20,880 m/week (SD=13,230) vs. 7486 m/week (SD=4936) in periods during which no such winds were recorded. Serological evidence demonstrated exposure to the virus up to 166 km away from the location of the initial outbreak center. Modeled wind data showed that this spread may be explained by winds at high altitudes. Animal movements due to shipments of feedlot calves and slaughters could not explain the spread pattern observed during the outbreak. This study therefore shows that winds are probably a major contributory factor for long and medium distance spread of Culicoides borne viruses in this region.
... The discovery of a novel virulent EHDV-8 strain in Tunisia (Sghaier et al., 2022), set in motion the upscaling of novel detection methods for this virus due to North Africa's proximity to Europe and the well-known cross-continental spread of infected biting midges via sandstorms to Europe (Kedmi et al., 2010;Lorusso et al., 2013;Lorusso et al., 2014;Sghaier et al., 2017). Indeed, in fall 2022, EHDV-8 strains with a 99.9% whole genome nucleotide sequence identity to the Tunisian prototype strain EHDV-8/17 TUN2021 were discovered in Sicily and Sardinia (Italy) in symptomatic cattle . ...
... To date, several EHDV serotyping PCR-based assays targeting the S2 have been developed and validated (Yadin et al., 2008;Allison et al., 2010;Kedmi et al., 2010). All these serotyping assays showed good sensitivity and specificity; however, due to the high variability found within the S2 region, novel EHDV strains are likely to have changes in primer or probe binding sites used in these assays, therefore attention should be given to the redesigning and redefining of primers to cater to current circulating strains (Maan et al., 2012). ...
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Epizootic hemorrhagic disease virus (EHDV) is a Culicoides-transmitted virus circulating in multiple serotypes. It has become a concern in the European Union as a novel strain of the serotype 8 (EHDV-8) of clear Northern African origin, has been recently discovered in symptomatic cattle in Italy (islands of Sardinia and Sicily), Spain, and Portugal. Current molecular typing methods targeting the S2 nucleotide sequences -coding for the outermost protein of the virion-VP2- are not able to detect the novel emerging EHDV-8 strain as they considered the S2 sequence of the unique EHDV-8 reference strain isolated in Australia in 1982. Thus, in this study, we developed and validated a novel typing assay for the detection and quantitation of the novel EHDV-8 RNA from field samples, including blood of ruminants and insects. This molecular tool will certainly support EHDV-8 surveillance and control.
... A polymerase chain reaction (PCR) [34] was used in an amplifier to amplify specific DNA fragments, and could be used for bacteria or virus detection with strong specificity, high sensitivity, and low purity requirements. Maan et al. [66] reported a real-time reverse transcription polymerase chain reactions (RT-PCR) assay to recognize Seg-2 of the eight epizootic hemorrhagic disease virus (EHDV) serotypes [67,68]. However, such detectors are difficult to implement for point-of-care testing. ...
... Due to the Debye-Hückel screening effect [88], a highly sensitive strategy should be taken for biomarker detection during cancer [17] and infectious disease [68] testing. In this paper, we discussed the development process of the SiNW-FET biosensor. ...
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As a new type of one-dimensional semiconductor nanometer material, silicon nanowires (SiNWs) possess good application prospects in the field of biomedical sensing. SiNWs have excellent electronic properties for improving the detection sensitivity of biosensors. The combination of SiNWs and field effect transistors (FETs) formed one special biosensor with high sensitivity and target selectivity in real-time and label-free. Recently, SiNW-FETs have received more attention in fields of biomedical detection. Here, we give a critical review of the progress of SiNW-FETs, in particular, about the reversible surface modification methods. Moreover, we summarized the applications of SiNW-FETs in DNA, protein, and microbial detection. We also discuss the related working principle and technical approaches. Our review provides an extensive discussion for studying the challenges in the future development of SiNW-FETs.
... In Europe, significant outbreaks of BT resulted in high mortality in sheep and cattle (>1 million) as the disease shifted further north and became emergent in the region (Purse et al., 2005). These outbreaks of BT have been linked to climate change and shifting wind patterns affecting Culicoides distribution and virus transmission (Guis et al., 2012;Hartemink et al., 2009;Kedmi et al., 2010;Purse et al., 2005;Wilson & Mellor, 2008;Wittmann & Baylis, 2000). Likewise, cattle disease associated with EHDV infections has been reported in North America, Australia, the Middle East, Asia, and northern Africa (Gür, 2008;Kedmi et al., 2010;MacLachlan & Guthrie, 2010;Madani et al., 2011). ...
... These outbreaks of BT have been linked to climate change and shifting wind patterns affecting Culicoides distribution and virus transmission (Guis et al., 2012;Hartemink et al., 2009;Kedmi et al., 2010;Purse et al., 2005;Wilson & Mellor, 2008;Wittmann & Baylis, 2000). Likewise, cattle disease associated with EHDV infections has been reported in North America, Australia, the Middle East, Asia, and northern Africa (Gür, 2008;Kedmi et al., 2010;MacLachlan & Guthrie, 2010;Madani et al., 2011). ...
Article
Bluetongue virus (BTV) and epizootic hemorrhagic disease virus (EHDV) are globally distributed, vector‐borne viruses that infect and cause disease in domestic and wild ruminant species. The forces driving increases in resulting hemorrhagic disease (HD) may be linked to weather conditions and increasing severity has been noted in northerly latitudes. We evaluated the role of drought severity in both space and time on changes in HD reports across the eastern US for a recent 15‐year period. The objectives of this study were to: 1) develop a spatiotemporal model to evaluate if drought severity explains changing patterns of HD presence; and 2) to determine if this potential risk factor varies in importance over the present range of HD in the eastern US. Historic data (2000‐2014) from an annual HD presence‐absence survey conducted by the Southeastern Cooperative Wildlife Disease Study and from the United States Drought Monitor were used for this analysis. For every county in 23 states and for each of 15 years, data were based on reported drought status for August, wetland cover, the physiographic region, and the status of HD in the previous year. We used a generalized linear mixed model to explain HD presence and evaluated the spatiotemporal predictors across the region. We found that drought severity was a significant predictor of HD presence and the significance of this relationship was dependent on latitude. In more northerly latitudes, where immunological naivety is most likely, we demonstrated the increasing strength of drought severity as a determinant of reported HD and established the importance of variation in drought severity as a risk factor over the present range of HD in the eastern United States. Our research provides spatially explicit evidence for the link between climate forces and emerging disease patterns across latitude for a globally distributed disease.
... Up to 80% mortality has been recorded on affected deer farms in the United States (Lee and English 2011). The virus can infect cattle, and while infection is typically subclinical, the virus has been shown to result in productivity losses within the dairy industry (Kedmi et al. 2010a). The susceptibility and role of many ruminant species in EHDV epidemiology is still unknown. ...
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Orbiviruses are of significant importance to the health of wildlife and domestic animals worldwide; the major orbiviruses transmitted by multiple biting midge (Culicoides) species include bluetongue virus, epizootic hemorrhagic disease virus, and African horse sickness virus. The viruses, insect vectors, and hosts are anticipated to be impacted by global climate change, altering established Orbivirus epidemiology. Changes in global climate have the potential to alter the vector competence and extrinsic incubation period of certain biting midge species, affect local and long-distance dispersal dynamics, lead to range expansion in the geographic distribution of vector species, and increase transmission period duration (earlier spring onset and later fall transmission). If transmission intensity is associated with weather anomalies such as droughts and wind speeds, there may be changes in the number of outbreaks and periods between outbreaks for some regions. Warmer temperatures and changing climates may impact the viral genome by facilitating reassortment and through the emergence of novel viral mutations. As the climate changes, Orbivirus epidemiology will be inextricably altered as has been seen with recent outbreaks of bluetongue, epizootic hemorrhagic disease, and African horse sickness outside of endemic areas, and requires interdisciplinary teams and approaches to assess and mitigate future outbreak threats.
... These results support the scenario of the inter-continental BEFV virus spread (22,24). Wind transport of infected vectors over long distances is a scenario considered for past BEF epizootics (24)(25)(26) (1). Increasing virus controls with BEFV screening in the host and limiting free animal crossings between Turkey and border countries may limit the spread of BEFV. ...
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Bovine ephemeral fever (BEF) is a vector-borne disease of ruminants in tropical and subtropical areas, leading to significant economic losses to the cattle and milk industry in many countries, including Turkey. Cattle showing high fever, stagnation, and recumbency have been extensively reported in Turkey's south and south eastern regions in 2020. Here, the genetic analysis and molecular epidemiology of the virus obtained from the last BEF outbreak were investigated. Of 32 symptomatic cattle selected from three provinces in Turkey, 23 were positive for bovine ephemeral fever virus (BEFV), and three entire G genes were identified by sequencing. The new BEFV isolates were genetically similar to some Turkish and Israeli isolates from 2008 and 2012 (>98 nucleotide (nt), 97% amino acid (aa)), and phylogenetic analysis based on the surface glycoprotein (G) gene revealed that BEFV isolates are of Middle Eastern origin. The G protein amino acid alignment showed that BEFV circulated in the same region with minor differences over the years. In this context, we recommend closely monitoring BEF outbreaks in neighbouring countries and prompt vaccination of susceptible cattle in areas at risk for BEFV in Turkey in the event of an outbreak.
... However, there is no evidence of the virus overwintering in northern areas; therefore, this remains to be evaluated. During the 2006 EHDV outbreak in Israel, winds were considered a major contributing factor to HD spread 71 . Additionally, the maintenance of BTV in a farm in temperate regions in northern California was associated with prolonged survival of C. sonorensis, thus contributing to interseason maintenance 72 . ...
Article
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Epizootic hemorrhagic disease (EHD) and bluetongue (BT) are vector-borne viral diseases that affect wild and domestic ruminants. Clinical signs of EHD and BT are similar; thus, the syndrome is referred to as hemorrhagic disease (HD). Syndromic surveillance and virus detection in North America reveal a northern expansion of HD. High mortalities at northern latitudes suggest recent incursions of HD viruses into northern geographic areas. We evaluated the occurrence of HD in wild Illinois white-tailed deer from 1982 to 2019. Our retrospective space–time analysis identified high-rate clusters of HD cases from 2006 to 2019. The pattern of northward expansion indicates changes in virus-host-vector interactions. Serological evidence from harvested deer revealed prior infection with BTV. However, BTV was not detected from virus isolation in dead deer sampled during outbreaks. Our findings suggest the value of capturing the precise geographic location of outbreaks, the importance of virus isolation to confirm the cause of an outbreak, and the importance of expanding HD surveillance to hunter-harvested wild white-tailed deer. Similarly, it assists in predicting future outbreaks, allowing for targeted disease and vector surveillance, helping wildlife agencies communicate with the public the cause of mortality events and viral hemorrhagic disease outcomes at local and regional scales.
... Furthermore, the expansion of BTV into areas where the main vector, C. imicola, is rare or absent suggests the involvement of previously unidentified indigenous European Culicoides species (e.g., the Culicoides obsoletus group and Culicoides pulicaris group) that were widespread and abundant [121]. In addition, the expansion of the geographic distribution of BTV to north-central Europe starting in 2006 has been linked to climate change and shifting wind patterns affecting Culicoides distribution and virus transmission [122,123]. ...
Article
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Bluetongue (BT) and epizootic hemorrhagic disease (EHD) cases have increased worldwide, causing significant economic loss to ruminant livestock production and detrimental effects to susceptible wildlife populations. In recent decades, hemorrhagic disease cases have been reported over expanding geographic areas in the United States. Effective BT and EHD prevention and control strategies for livestock and monitoring of these diseases in wildlife populations depend on an accurate understanding of the distribution of BT and EHD viruses in domestic and wild ruminants and their vectors, the Culicoides biting midges that transmit them. However, national maps showing the distribution of BT and EHD viruses and the presence of Culicoides vectors are incomplete or not available at all. Thus, efforts to accurately describe the potential risk of these viruses on ruminant populations are obstructed by the lack of systematic and routine surveillance of their hosts and vectors. In this review, we: (1) outline animal health impacts of BT and EHD in the USA; (2) describe current knowledge of the distribution and abundance of BT and EHD and their vectors in the USA; and (3) highlight the importance of disease (BT and EHD) and vector surveillance for ruminant populations.
... High wind velocity can improve ventilation and air quality, which would reduce exposure to E. rhusiopathiae. Furthermore, it may affect the spread of arthropod borne diseases through active or passive dispersal of their vectors [35]. Additionally, it might contribute to the evaporation of humidity and heat radiation inside the barn. ...
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Swine erysipelas (SE) is one of the best-known and most serious diseases that affect domestic pigs, which is caused by Erysipelothrix rhusiopathiae. It is endemic in Nanning and has been circulating for decades, causing considerable economic losses. The aim of this study was to investigate the effect of meteorological-related variations on the epidemiology of swine erysipelas in Nanning City, a subtropical city of China. Data on monthly counts of reported swine erysipelas and climate data in Nanning are provided by the authorities over the period from 2006 to 2015. Cross-correlation analysis was applied to identify the lag effects of meteorological variables. A zero-inflated negative binomial (ZINB) regression model was used to evaluate the independent contribution of meteorological factors to SE transmission. After controlling seasonality, autocorrelation and lag effects, the results of the model indicated that Southern Oscillation Index (SOI) has a positive effect on SE transmission. Moreover, there is a positive correlation between monthly mean maximum temperature and relative humidity at 0-1 month lag and the number of cases. Furthermore, there is a positive association between the number of SE incidences and precipitation, with a lagged effect of 2 months. In contrast, monthly mean wind velocity negatively correlated with SE of the current month. These findings indicate that meteorological variables may play a significant role in SE transmission in southern China. Finally, more public health actions should be taken to prevent and control the increase of SE disease with consideration of local weather variations.
... Wild deer populations surrounding this farm may have had a greater prevalence of EHDV-2 than farmed populations leading to the dissimilarities in serotype distribution between deer and midges on this property. Culicoides are also believed to travel on wind currents [41,42], which could have transported midges from an area experiencing greater EHDV-2 activity towards the Jefferson County farm. Finally, this result could also be attributable to stochasticity due to low sample sizes of EHDV positive animals available for sampling at the time of death. ...
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Background: Epizootic hemorrhagic disease virus (EHDV) is an Orbivirus of veterinary importance which is transmitted by biting midges of the genus Culicoides (Diptera: Ceratopogonidae) to ruminants. Culicoides sonorensis Wirth & Jones, the only confirmed vector of EHDV in the USA, is rare in the southeastern states where transmission persists, suggesting that other Culicoides species transmit EHDV in this region. The present study aimed to determine which Culicoides species transmitted EHDV in Florida and Alabama, two states in the southeastern USA. Viral RNA was detected in field-collected midges using molecular methods. These data are presented alongside data on Culicoides blood meal analysis, white-tailed deer (Odocoileus virginianus) aspiration, and seasonality to demonstrate an interaction between potential vector species and EHDV hosts. Results: Out of 661 pools tested, 20 pools were positive for EHDV viral RNA, including six pools from Culicoides stellifer (Coquillett) and 14 pools from Culicoides venustus Hoffman. The overall infection rate was 0.06% for C. stellifer and 2.18% for C. venustus. No positive pools were identified for a further 17 species. Serotypes identified in Culicoides included EHDV-2, EHDV-6, and coinfections of EHDV-2 and EHDV-6 and were identified in similar proportions to serotypes in deer at 3 of 4 deer farms. Viral detections conducted in Alabama also identified one positive pool of C. venustus. Blood meal analysis revealed that both Culicoides species fed on white-tailed deer (verified through aspiration), fallow deer, and elk, species for which EHDV viremia has been documented. Seasonality data indicated that both species were present throughout the period in which viral transmission occurred to EHDV hosts in 2016 in addition to the 2017 epizootic. Conclusions: Our finding of EHDV positive pools of field-collected C. stellifer and C. venustus and an interaction between these species and EHDV hosts satisfy two of the four criteria for vector incrimination as set by the World Health Organization. Determining the vectors of EHDV is an important step towards developing sound strategies for the control of vector Culicoides and management of EHDV in the southeastern USA.
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The effect of climatic factors on the presence of Culicoides Latreille (Diptera: Ceratopogonidae) was previously studied. Nevertheless, lack of laboratory rearing data hampers species‐specific prediction of weather fluctuations effect on population size. To determine fluctuations in population size in the field, we recorded Culicoides and other Nematocerans in seven Israeli dairy farms over two‐years (2011–2012) and analysed the association of their dynamics with fluctuations in ambient temperature and total rainfall. In six farms, the most abundant species were Culicoides imicola Kieffer and Culicoides schultzei (Enderlein) gp., primarily composed of parous females, and in one farm Culicoides obsoletus (Meigen) gp., mostly nulliparous females, were dominant. While the total number of insects was similar in both years, Culicoides numbers were significantly higher in 2012, but appeared later in the season and reached a higher peak. A multi‐variable linear regression model demonstrated positive association of C. imicola and C. schultzei numbers with the monthly multi‐annual ambient temperature and its specific deviation, but not with monthly rainfall. C. obsoletus populations peaked at spring and sharply decreased when temperature exceeded 20 °C, and were best modelled by adding quadratic terms. Weather‐specific estimation of population size under field conditions may enable to predict outbreaks intensity of Culicoides‐borne viruses.
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In 2006, over 2000 cases of bluetongue were recorded in northern Europe. The disease, which has been more typically associated with Mediterranean areas, is believed to have become established hundreds of kilometres to the north of its traditional area, probably as a consequence of the hottest summer/autumn period since records began. In this special article, John Gloster and colleagues describe the meteorological conditions surrounding the 2006 outbreak, and investigate the possibility of bluetongue virus (BTV) spreading on the wind to the UK in 2007. For this to happen there would need to be a source of windborne virus, together with a susceptible population of ruminants in the vicinity of the coast. Evidence from outbreaks in the Mediterranean Basin suggests that long-distance transport of BTV-infected vectors has already occurred, at least in that region. The overall likelihood of this occurring in northern Europe depends critically on whether the virus overwinters on the near continent; this will not be known until around May 2007. The 2006 outbreak has highlighted the importance of understanding the impact of climate change on animal disease.
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Epizootic hemorrhagic disease is caused by a Culicoides-borne Orbivirus. In cattle, the disease is characterized by reduced milk production and mortality. Recent outbreaks of epizootic hemorrhagic disease virus (EHDV) in North Africa, Israel, and Turkey increase the risk of its invasion into central and northern Europe. An outbreak of EHDV in Israel during the fall of 2006 enabled an assessment of the consequent production losses to the dairy cattle industry. Reduction in milk production and involuntary culling were modeled using a 4-yr database of monthly milk and mortality records from 48 affected and 63 unaffected herds. These indices were compared between periods of outbreak and no outbreak and assessed for various levels and exposure onset. Geospatial kriging interpolation of serological results from 127 herds was used to assess the total outbreak losses for the dairy cattle industry in Israel. Herds affected during the first, second, and third month of the outbreak (September-November) experienced an average loss of 207 (95% CI=154-261), 137 (63-211), and 52 (27-76) kg of milk/milking cow, respectively, during the outbreak period. An average excess mortality and involuntary culling of 1.47/100 cows was documented in herds affected in September. High correlation was observed between EHDV seroprevalence and milk loss; average milk loss for herds with seropositivity of 26 to 50, 51 to 75, and 76 to 100% was 84, 133, and 204 kg of milk/milking cow, respectively. A 1.42% (0.91-1.93%) increase in mortality was observed in herds with seroprevalence above 50%. Losses for the dairy cattle industry interpolated from these data were estimated at US2,491,000(US2,491,000 (US1,591,000-3,391,000), an average loss of US$26.5/cow in the Israeli dairy cattle. This equals 0.55% of the average total value production of a dairy cow in Israel. This is the first study to estimate the production losses caused by EHDV or any bluetongue-like disease.
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Observations were made of clinical signs, gross and microscopic lesions in white-tailed deer infected with epizootic hemorrhagic disease (EHD) virus. Typically, animals became weak and lethargic and developed hyperemia of the oral and nasal mucosa, tongue, ears and sclera of the eyes six to seven days following intramuscular inoculation with virus. Body temperature increased initially and then fell to subnormal levels just prior to death.A decrease in levels of circulating blood platelets was correlated with the occurrence of fever and the appearance of platelet and fibrin thrombi in small vessels of many organs of the body. Thrombosis resulted in tissue degeneration, necrosis and hemorrhages in the terminal stages of the disease. Tissues most seriously affected were oral, nasal and tongue mucosa, mandibular salivary glands, myocardium and epithelium of the forestomachs. The lesions resembled those of blue-tongue in deer. Inoculation of domestic sheep with EHD virus-infected deer spleen tissues was without clinical effect. Blood collected from the sheep, representing the third blind passage of EHD virus in sheep, was not infective for deer.
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A competitive enzyme-linked immunosorbent assay is described for the detection of antibodies against epizootic haemorrhagic disease of deer viruses (EHDV). Test antisera were tested against a guinea-pig antiserum raised against EHDV core particles. The assay detected antibodies to all serotypes of EHDV, but unlike the agar gel immunodiffusion (AGID) test, gave no cross-reactions with antibodies against bluetongue, Palyam and Tilligery viruses. The C-ELISA would be ideal for use in epidemiological surveys since it is suitable for the examination of antisera from all susceptible species without the need for individual species-specific enzyme conjugates.
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A monoclonal antibody based competitive enzyme-linked immunosorbent assay (MC-ELISA) for the detection of antibodies against epizootic haemorrhagic disease of deer viruses (EHDV) is described. Test sera were competed with a monoclonal antibody against the VP7 protein of EHDV serotype 1. The assay was capable of detecting antibodies to all serotypes of EHDV but unlike the agar gel immunodiffusion (AGID) test, gave no cross-reactions with antibodies against bluetongue, Palyam or Tilligery viruses. The MC-ELISA was more sensitive than a polyclonal based ELISA reported previously (Thevasagayam et al., 1995b) and would be ideal for epidemiological surveys since it is suitable for the examination of antisera from all animal species without the need for individual anti-species enzyme conjugates.
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To evaluate the vector competence of Culicoides lahillei Lutz for epizootic hemorrhagic disease (EHD) viruses, wild-caught females were allowed to feed on 4 viremic white-tailed deer, Odocoileus virginianus Zimmermann, experimentally infected with EHD virus serotype 2 (EHDV-2). Colonized C. variipennis sonorensis (Coquillett) were included as a positive control. Virus was not isolated from 13 C. lahillei tested 4-15 d after feeding on deer with viremias of 3.0 or <2.1 log10 tissue culture infectious dose50 (TCID50) virus per milliliter of blood. Virus was isolated from 6 of 69 (8.7%) C. lahillei tested 4-15 d after feeding on deer with viremias of 5.3 or 6.0 TCID50 virus per milliliter of blood. The average amount of EHDV-2 ingested in the blood meal ranged from <log10 1.5 to log10 1.9 TCID50 per C. lahillei. Titers of EHDV-2 in C. lahillei that tested positive 4-15 d after feeding peaked at log10 2.7 TCID50 EHDV per fly. Replication of EHDV-2 also occurred in control C. variipennis. This report of infection of C. lahillei with an EHD virus serotype indicates that C. lahillei may be a vector of EHD viruses.