Studying Culicoides vectors of BTV in the post-genomic era: Resources, bottlenecks to progress and future directions

Nayduch, Dana; Cohnstaedt, Lee W.; Saski, Christopher; Lawson, Daniel; Kersey, Paul J.; Fife, Mark; Carpenter, Simon

doi:10.1016/j.virusres.2013.12.009

Cited by 54 publications

(63 citation statements)

References 64 publications

(87 reference statements)

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“…Unlike the original method, which relied upon the use of populations in close proximity to contained facilities, the technique had the advantage of including an incubation step that precluded the inclusion of naturally blood-fed individuals from traps and can be used with light-suction trap collections from a wide geographical area. While blood-feeding rates remained poor, this development is useful in creating a platform for both vector competence experimentation and wider vectorvirus interaction studies in addition to laboratory-based studies of bionomics for which little data is available for the subgenus Avaritia in northwestern Europe [32].…”

Section: Discussionmentioning

confidence: 99%

“…A key research limitation, however, is that techniques have not been developed to artificially blood-feed field-collected species of Palaearctic Culicoides through membranes under conditions of biological containment [30,31]. This not only limits studies attempting to standardise population susceptibility to infection across the region, but also prevents the establishment of colony and cell lines of these species as a resource [32].…”

Section: Introductionmentioning

confidence: 99%

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Blood-feeding, susceptibility to infection with Schmallenberg virus and phylogenetics of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom

Barber¹,

Harrup²,

Silk³

et al. 2018

Parasites Vectors

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Background: Culicoides biting midges (Diptera: Ceratopogonidae) are responsible for the biological transmission of internationally important arboviruses of livestock. In 2011, a novel Orthobunyavirus was discovered in northern Europe causing congenital malformations and abortions in ruminants. From field studies, Culicoides were implicated in the transmission of this virus which was subsequently named Schmallenberg virus (SBV), but to date no assessment of susceptibility to infection of field populations under standardised laboratory conditions has been carried out. We assessed the influence of membrane type (chick skin, collagen, Parafilm M®) when offered in conjunction with an artificial blood-feeding system (Hemotek, UK) on field-collected Culicoides blood-feeding rates. Susceptibility to infection with SBV following blood-feeding on an SBV-blood suspension provided via either (i) the Hemotek system or via (ii) a saturated cotton wool pledglet was then compared. Schmallenberg virus susceptibility was defined by RT-qPCR of RNA extractions of head homogenates and related to Culicoides species and haplotype identifications based on the DNA barcode region of the mitochondrial cytochrome c oxidase 1 (cox1) gene. Results: Culicoides blood-feeding rates were low across all membrane types tested (7.5% chick skin, 0.0% for collagen, 4.4% Parafilm M®, with 6029 female Culicoides being offered a blood meal in total). Susceptibility to infection with SBV through membrane blood-feeding (8 of 109 individuals tested) and pledglet blood-feeding (1 of 94 individuals tested) was demonstrated for the Obsoletus complex, with both C. obsoletus (Meigen) and C. scoticus Downes & Kettle susceptible to infection with SBV through oral feeding. Potential evidence of cryptic species within UK populations was found for the Obsoletus complex in phylogenetic analyses of cox1 DNA barcodes of 74 individuals assessed from a single field-site. Conclusions: Methods described in this study provide the means to blood-feed Palaearctic Culicoides for vector competence studies and colonisation attempts. Susceptibility to SBV infection was 7.3% for membrane-fed members of the subgenus Avaritia and 1.1% for pledglet-fed. Both C. obsoletus and C. scoticus were confirmed as being susceptible to infection with SBV, with potential evidence of cryptic species within UK Obsoletus complex specimens, however the implications of cryptic diversity in the Obsoletus complex on arbovirus transmission remains unknown.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Blood-feeding, susceptibility to infection with Schmallenberg virus and phylogenetics of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom

Barber¹,

Harrup²,

Silk³

et al. 2018

Parasites Vectors

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“…Efforts toward laboratory colonization of alternate Culicoides vector species should be intensified, as vector competence studies have largely focused on colonized C. sonorensis both in the United States and the United Kingdom. Although the utilization of molecular methods for the study of Culicoides vector biology has expanded very recently (Nayduch et al 2014a), these tools have not yet been brought to bear on control tactics. However, the recent release of the C. sonorensis reference transcriptome (Nayduch et al 2014b) as well as a demonstration of RNA interference (RNAi) in vivo (Mills et al 2015) present new tools in the molecular biological toolbox to use in vector competence studies.…”

Section: Control Of Disease Through Manipulations Of Vector Competencementioning

confidence: 99%

Management of North American Culicoides Biting Midges: Current Knowledge and Research Needs

Pfannenstiel

Mullens

Ruder

et al. 2015

Vector-Borne and Zoonotic Diseases

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Culicoides biting midges (Diptera: Ceratopogonidae) are biological vectors of two important viruses impacting North American ruminants--bluetongue virus (BTV) and epizootic hemorrhagic disease virus (EHDV). These viruses have been identified for over 60 years in North America, but we still lack an adequate understanding of the basic biology and ecology of the confirmed vector, Culicoides sonorensis, and know even less about other putative Culicoides vector species. The major gaps in our knowledge of the biology of Culicoides midges are broad and include an understanding of the ecology of juveniles, the identity of potential alternate vector species, interactions of midges with both pathogens and vertebrates, and the effectiveness of potential control measures. Due to these broad and numerous fundamental knowledge gaps, vector biologists and livestock producers are left with few options to respond to or understand outbreaks of EHD or BT in North America, or respond to emerging or exotic Culicoides-transmitted pathogens. Here we outline current knowledge of vector ecology and control tactics for North American Culicoides species, and delineate research recommendations aimed to fill knowledge gaps.

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“…The functional dependence of biting frequency [31] and life expectancy [32] upon temperature has been quantified for Culicoides sonorensis. Although these functional relations are derived for only one midge species, in part because of serious technical challenges in the laboratory colonization of midge species [33], they are widely used in the recent BTV mechanistic modelling literature [34][35][36][37][38]. BTV develops within infected midges more rapidly at higher temperatures and therefore the extrinsic incubation period (EIP) between the bite that infected a midge and when subsequent midge bites are infectious is shorter at higher temperatures.…”

Section: Introductionmentioning

confidence: 99%

The impact of temperature changes on vector-borne disease transmission: Culicoides midges and bluetongue virus

Brand

Keeling

2017

J. R. Soc. Interface.

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It is a long recognized fact that climatic variations, especially temperature, affect the life history of biting insects. This is particularly important when considering vector-borne diseases, especially in temperate regions where climatic fluctuations are large. In general, it has been found that most biological processes occur at a faster rate at higher temperatures, although not all processes change in the same manner. This differential response to temperature, often considered as a trade-off between onward transmission and vector life expectancy, leads to the total transmission potential of an infected vector being maximized at intermediate temperatures. Here we go beyond the concept of a static optimal temperature, and mathematically model how realistic temperature variation impacts transmission dynamics. We use bluetongue virus (BTV), under UK temperatures and transmitted by Culicoides midges, as a well-studied example where temperature fluctuations play a major role. We first consider an optimal temperature profile that maximizes transmission, and show that this is characterized by a warm day to maximize biting followed by cooler weather to maximize vector life expectancy. This understanding can then be related to recorded representative temperature patterns for England, the UK region which has experienced BTV cases, allowing us to infer historical transmissibility of BTV, as well as using forecasts of climate change to predict future transmissibility. Our results show that when BTV first invaded northern Europe in 2006 the cumulative transmission intensity was higher than any point in the last 50 years, although with climate change such high risks are the expected norm by 2050. Such predictions would indicate that regular BTV epizootics should be expected in the UK in the future.

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Studying Culicoides vectors of BTV in the post-genomic era: Resources, bottlenecks to progress and future directions

Cited by 54 publications

References 64 publications

Blood-feeding, susceptibility to infection with Schmallenberg virus and phylogenetics of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom

Blood-feeding, susceptibility to infection with Schmallenberg virus and phylogenetics of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom

Management of North American Culicoides Biting Midges: Current Knowledge and Research Needs

The impact of temperature changes on vector-borne disease transmission: Culicoides midges and bluetongue virus

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