The combination of abundance and infection rates of Culicoides sonorensis estimates risk of subsequent bluetongue virus infection of sentinel cattle on California dairy farms

Abstract

Bluetongue is an important viral disease of ruminants that is transmitted by hematophagous Culicoides midges. We examined the seasonal patterns of abundance and infection of Culicoides sonorensis (C. sonorensis) at 4 dairy farms in the northern CentralValley of California to develop estimates of risk for BTV transmission to sentinel cattle at each farm. These 4 farms were selected because of their similar meteorological conditions but varying levels of vector abundance and BTV infection of cattle (Mayo et al., 2011). C. sonorensis midges were collected weekly at each farm during the seasonal transmission period, using three different trapping methods: traps baited with either carbon dioxide (CO 2 ) alone or traps with CO 2 and UV light, and by direct aspiration of midges from sentinel cattle. Analysis of BTV-infected midges using group and serotypespecific quantitative reverse-transcriptase polymerase chain reaction (qRT-PCR) assays confirmed that BTV serotypes 10, 11, 13 and 17 are all present in the region, but that midge infection rates and the number of BTV serotypes circulating differed markedly among the individual farms. Furthermore, more serotypes of BTV were present in midges than in sentinel cattle at individual farms where BTV circulated, and the virus was detected at each farm in midges prior to detection in cattle. BTV infection rates were remarkably lower amongst female C. sonorensis midges collected by CO 2 traps with UV light than among midges collected by either animal-baited aspirations or in CO 2 traps without light. A subsample of female midges examined from each collection method showed no overall differences in the proportion of female midges that had previously fed on a host. Findings from this study confirm the importance of using sensitive 3 surveillance methods for both midge collection and virus detection in epidemiological studies of BTV infection, which is especially critical if the data are to be used for development of mathematical models to predict the occurrence of BTV infection of livestock.

Seasonal and Interseasonal Dynamics of Bluetongue Virus Infection of Dairy Cattle and Culicoides sonorensis Midges in Northern California – Implications for Virus Overwintering in Temperate Zones

“…Ongoing surveillance since that time, including our studies, has confirmed that BTV infection of ruminant livestock in California is endemic but highly seasonal (late July – November), thus the interseasonal period (November – July) when BTV is apparently “inactive” lasts approximately 8 months [9], [15], [16], [17]. In the current study we undertook intensive surveillance of sentinel cattle and vector midges during both the seasonal and interseasonal periods of BTV activity at a dairy farm in Northern California (latitude 39.590° N).…”

“…Collection of adult midges was repeated during a portion of the interseasonal period of 2014 (January-March) on the transect where 32 parous females had been collected in 3 different traps during Feb 2013, and on another transect where no interseasonal activity of midges was detected during 2013. Trapping was performed weekly in 2014 with the addition of 3 tent - type emergence traps set and rotated weekly along the edge of the waste-water lagoon, a known larval habitat [9]. The emergence traps were constructed of no-seeum netting (Bioquip Products) securely fastened over polyvinyl chloride (PVC) pipe.…”

“…Viral RNA was extracted from the homogenate using the viral RNA isolation kit (AM1836, Ambion) according to the manufacturer's recommendations. The presence of BTV in the homogenated midge pools was determined by quantitative reverse transcriptase polymerase chain reaction (qRT-PCR) amplification and detection of the BTV S10 gene, as previously described [9]. Lysates of pooled C. sonorensis midges collected during the interseasonal period were run in duplicate and the assays repeated to confirm the findings.…”

“…Whole blood samples from animals that tested positive by cELISA were then screened for the presence of viral RNA by BTV-specific qRT-PCR so that the approximate date (by week) of BTV infection could be estimated based on the date of the first blood collection in which viral RNA was detected, as previously described [9].…”

“…It has been proposed that the recent emergence of BTV in Europe is linked to climate change, likely through the effects of temperature on the biology of the midges that serve as biological vectors of BTV and the rate of BTV replication within its insect host [3], [6], [7]. Bluetongue virus infection of animals at temperate latitudes is distinctly seasonal (typically July – November in the Northern Hemisphere) but it remains uncertain how BTV persists during winter months when cold temperatures restrict vector activity and reproduction [8], [9]. The mechanism of this so-called “overwintering” of BTV in endemic temperate regions has vexed scientists since the original published descriptions of BT in South Africa over a century ago [10].…”