Virus-Vector-Host Interactions of Culicoides-Borne Diseases

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Invertebrate Viruses".

Deadline for manuscript submissions: closed (31 March 2019) | Viewed by 79613

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Guest Editor
National Bio and Agro-Defense Facility, USDA Agricultural Research Service (ARS), Manhattan, KS 66502, USA
Interests: arthropod-borne animal diseases; arbovirus; culicoides-borne viruses; insect vectors; virus–vector interactions; rift valley fever virus
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Guest Editor
United States Department of Agriculture, Agricultural Research Service, Arthropod Borne Animal Disease Research Unit, 1515 College Ave., Manhattan, KS 66502, USA
Interests: Arthropod-borne animal diseases; arbovirus; Culicoides-Borne viruses; insect vectors; insect salivary proteins; virus-vector-host interations; Orbiviruses; Rift Valley Fever virus; Japanese encephalitis virus; vesicular stomatitis virus
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Culicoides biting midges are important world-wide public health and agricultural pests that transmit several emerging and re-emerging arboviruses causing economically significant losses from infected humans, livestock, and wildlife. The Culicoides-borne arboviruses include African horse sickness, bluetongue, and epizootic hemorrhagic disease viruses (Orbivirus), Schmallenberg, Akabane, Oropouche viruses (Orthobunyavirus), and vesicular stomatitis and bovine ephemeral fever viruses (Rhabdoviridae). Although Culicoides biting midges have been recognized as important arboviral vectors for more than half a century, much is still unknown about the interactions between viruses, vectors, and infected hosts. The emergence and recent re-emergence of one of these arboviruses (bluetongue virus) in Europe have stimulated new interest in Culicoides-borne disease detection, surveillance, vaccine design, viral and vector genomics and proteomics, as well as integrated pest management of these important disease vectors.

This Special Issue on “Virus–Vector–Host Interactions of Culicoides-Borne Diseases” is open to all researchers working on Culicoides and Culicoides-borne viruses.

Papers are welcome as original research articles as well as review articles dealing with recent advancements and the current understanding of Culicoides-borne diseases.

Dr. William C. Wilson
Dr. Barbara S. Drolet
Guest Editors

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Keywords

  • Culicoides-borne diseases
  • African horse sickness
  • bluetongue
  • epizootic hemorrhagic disease
  • Schmallenberg
  • Akabane
  • Oropouche 
  • vesicular stomatitis
  • bovine ephemeral fever
  • vector biology
  • immunology
  • integrated pest management

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Published Papers (17 papers)

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Research

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18 pages, 883 KiB  
Article
Vector Competence of Italian Populations of Culicoides for Some Bluetongue Virus Strains Responsible for Recent Northern African and European Outbreaks
by Valentina Federici, Maria Goffredo, Giuseppe Mancini, Michela Quaglia, Adriana Santilli, Francesca Di Nicola, Matteo De Ascentis, Pierangela Cabras, Carmela Volpicelli, Claudio De Liberato, Giuseppe Satta, Giovanni Federico, Alessandra Leone, Maura Pisciella, Ottavio Portanti, Federica Pizzurro, Liana Teodori and Giovanni Savini
Viruses 2019, 11(10), 941; https://doi.org/10.3390/v11100941 - 12 Oct 2019
Cited by 21 | Viewed by 3348
Abstract
The distribution of Bluetongue virus (BTV) in Europe can be represented by two distinct and interconnected epidemiological systems (episystems), each characterized by different ecological characteristics and vector species. This study investigated the vector competence of Italian populations of Culicoides imicola and Culicoides obsoletus/scoticus [...] Read more.
The distribution of Bluetongue virus (BTV) in Europe can be represented by two distinct and interconnected epidemiological systems (episystems), each characterized by different ecological characteristics and vector species. This study investigated the vector competence of Italian populations of Culicoides imicola and Culicoides obsoletus/scoticus to some representative BTV strains after artificial oral infection. The BTV strains were selected according to their ability to spread to one or both episystems and included BTV-4 ITA, responsible of the recent Italian and French BTV-4 outbreaks; the BTV-2 strain which caused the first BTV incursion in Italy, Corsica, and Balearic Islands; BTV-4 MOR, responsible for the epidemic in Morocco; and BTV-8, the strain which spread through Europe between 2006 and 2008. Blood-soaked cotton pledgets and Hemotek membrane feeder using Parafilm® membrane were used to artificially feed midges. For each population/strain, recovery rates (positive/tested heads) were evaluated using serogroup- and serotype-specific RT-PCR. The trial demonstrated that, except for the Abruzzo population of C. obsoletus/C. scoticus, which was refractory to BTV-4 MOR infection, all the investigated Culicoides populations are susceptible to the selected BTV strains and that, if prompt vaccination programs and restriction measures had not been implemented, BTV-2 and BTV-4 MOR could have spread all over Europe. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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26 pages, 3041 KiB  
Article
Red deer (Cervus elaphus) Did Not Play the Role of Maintenance Host for Bluetongue Virus in France: The Burden of Proof by Long-Term Wildlife Monitoring and Culicoides Snapshots
by Sophie Rossi, Thomas Balenghien, Cyril Viarouge, Eva Faure, Gina Zanella, Corinne Sailleau, Bruno Mathieu, Jean-Claude Delécolle, Camille Ninio, Claire Garros, Laëtitia Gardès, Christophe Tholoniat, Agnès Ariston, Dominique Gauthier, Stevan Mondoloni, Aurélie Barboiron, Maryline Pellerin, Philippe Gibert, Corinne Novella, Stéphane Barbier, Etienne Guillaumat, Stéphan Zientara, Damien Vitour and Emmanuel Bréardadd Show full author list remove Hide full author list
Viruses 2019, 11(10), 903; https://doi.org/10.3390/v11100903 - 27 Sep 2019
Cited by 9 | Viewed by 3738
Abstract
Bluetongue virus (BTV) is a Culicoides-borne pathogen infecting both domestic and wild ruminants. In Europe, the Red Deer (Cervus elaphus) (RD) is considered a potential BTV reservoir, but persistent sylvatic cycle has not yet been demonstrated. In this paper, we [...] Read more.
Bluetongue virus (BTV) is a Culicoides-borne pathogen infecting both domestic and wild ruminants. In Europe, the Red Deer (Cervus elaphus) (RD) is considered a potential BTV reservoir, but persistent sylvatic cycle has not yet been demonstrated. In this paper, we explored the dynamics of BTV1 and BTV8 serotypes in the RD in France, and the potential role of that species in the re-emergence of BTV8 in livestock by 2015 (i.e., 5 years after the former last domestic cases). We performed 8 years of longitudinal monitoring (2008–2015) among 15 RD populations and 3065 individuals. We compared Culicoides communities and feeding habits within domestic and wild animal environments (51,380 samples). Culicoides diversity (>30 species) varied between them, but bridge-species able to feed on both wild and domestic hosts were abundant in both situations. Despite the presence of competent vectors in natural environments, BTV1 and BTV8 strains never spread in RD along the green corridors out of the domestic outbreak range. Decreasing antibody trends with no PCR results two years after the last domestic outbreak suggests that seropositive young RD were not recently infected but carried maternal antibodies. We conclude that RD did not play a role in spreading or maintaining BTV in France. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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13 pages, 1459 KiB  
Article
Field Evaluation of Deltamethrin and Ivermectin Applications to Cattle on Culicoides Host-Alighting, Blood-Feeding, and Emergence
by Archie K. Murchie, Geoff M. Thompson, Sam Clawson, Andrew Brown, Alan W. Gordon and Stephen Jess
Viruses 2019, 11(8), 731; https://doi.org/10.3390/v11080731 - 8 Aug 2019
Cited by 4 | Viewed by 4611
Abstract
The impact of topical applications of deltamethrin and ivermectin to cattle on Culicoides spp. landing and blood-feeding was studied in this work using sticky traps mounted on Friesian heifers’ backs. There was no effect of the insecticides on total numbers of Culicoides trapped [...] Read more.
The impact of topical applications of deltamethrin and ivermectin to cattle on Culicoides spp. landing and blood-feeding was studied in this work using sticky traps mounted on Friesian heifers’ backs. There was no effect of the insecticides on total numbers of Culicoides trapped or the proportion engorged. Deltamethrin and ivermectin treatment did not prevent blood-feeding on these animals. Deltamethrin did result in significant Culicoides mortality as evidenced by the numbers of dead midges combed from heifers’ upper flanks. The proximity of engorged midges on traps to dead midges in the hair suggests that blood-feeding took place despite midges receiving an ultimately lethal dose of deltamethrin. Ivermectin application resulted in a smaller proportion of nulliparous than parous females caught. There was no significant effect of ivermectin on the numbers of Culicoides that emerged from dung samples (but p was small at 0.095 for the Obsoletus group Culicoides). In cases of suspect animal imports, pour-on or spray applications of deltamethrin could reduce the risk of onward transmission of bluetongue virus. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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15 pages, 2603 KiB  
Article
Evidence of Intragenic Recombination in African Horse Sickness Virus
by Harry G. Ngoveni, Antoinette van Schalkwyk and J.J. Otto Koekemoer
Viruses 2019, 11(7), 654; https://doi.org/10.3390/v11070654 - 18 Jul 2019
Cited by 9 | Viewed by 4069
Abstract
Intragenic recombination has been described in various RNA viruses as a mechanism to increase genetic diversity, resulting in increased virulence, expanded host range, or adaptability to a changing environment. Orbiviruses are no exception to this, with intragenic recombination previously detected in the type [...] Read more.
Intragenic recombination has been described in various RNA viruses as a mechanism to increase genetic diversity, resulting in increased virulence, expanded host range, or adaptability to a changing environment. Orbiviruses are no exception to this, with intragenic recombination previously detected in the type species, bluetongue virus (BTV). African horse sickness virus (AHSV) is a double-stranded RNA virus belonging to the Oribivirus genus in the family Reoviridae. Genetic recombination through reassortment has been described in AHSV, but not through homologous intragenic recombination. The influence of the latter on the evolution of AHSV was investigated by analyzing the complete genomes of more than 100 viruses to identify evidence of recombination. Segment-1, segment-6, segment-7, and segment-10 showed evidence of intragenic recombination, yet only one (Segment-10) of these events was manifested in subsequent lineages. The other three hybrid segments were as a result of recombination between field isolates and the vaccine derived live attenuated viruses (ALVs). Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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15 pages, 1310 KiB  
Article
Emergence of a Novel Reassortant Strain of Bluetongue Serotype 6 in Israel, 2017: Clinical Manifestations of the Disease and Molecular Characterization
by Natalia Golender, Avi Eldar, Marcelo Ehrlich, Yevgeny Khinich, Gabriel Kenigswald, Joseph Seffi Varsano, Shachar Ertracht, Itzik Abramovitz, Itay Assis, Ily Shlamovitz, Eitan Tiomkin, Erez Yonay, Benny Sharir and Velizar Y. Bumbarov
Viruses 2019, 11(7), 633; https://doi.org/10.3390/v11070633 - 10 Jul 2019
Cited by 12 | Viewed by 3420
Abstract
Reassortment contributes to the evolution of RNA viruses with segmented genomes, including Bluetongue virus (BTV). Recently, co-circulation of natural and vaccine BTV variants in Europe, and their ensuing reassortment, were proposed to promote appearance of novel European BTV strains, with potential implications for [...] Read more.
Reassortment contributes to the evolution of RNA viruses with segmented genomes, including Bluetongue virus (BTV). Recently, co-circulation of natural and vaccine BTV variants in Europe, and their ensuing reassortment, were proposed to promote appearance of novel European BTV strains, with potential implications for pathogenicity, spread and vaccination policies. Similarly, the geographical features of the Mediterranean basin, which spans over portions of three continents, may facilitate the appearance of clinically relevant reassortants via co-circulation of BTV strains of African, Asian and European origins. In August–October 2017, BTV serotype 6 (BTV-6) was identified in young animals exhibiting classical clinical signs of Bluetongue (BT) at Israeli sheep and cattle farms. Sequencing and pairwise analysis of this Israeli BTV-6 isolate revealed the closest sequence homology of its serotype-defining Segment 2 was with that of South African reference BTV-6 strain 5011 (93.88% identity). In contrast, the other viral segments showed highest homology (97.0%–99.47% identity) with BTV-3, -4 and -9 of Mediterranean and African origins. Specifically, four viral segments were nearly identical (99.13%–99.47%), with Tunisian and Italian BTV-3 strains (TUN2016 and SAD2018, correspondingly). Together, our data suggest that Mediterranean co-circulation and reassortment of BTV-3 and BTV-6 drove the emergence of a novel and virulent BTV-6 strain Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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8 pages, 215 KiB  
Communication
Presence of Antibodies against Bluetongue Virus (BTV) in Sheep 5 to 7.5 Years after Vaccination with Inactivated BTV-8 Vaccines
by Johanna Hilke, Heinz Strobel, Soeren Woelke, Melanie Stoeter, Katja Voigt, Bernd Moeller, Max Bastian and Martin Ganter
Viruses 2019, 11(6), 533; https://doi.org/10.3390/v11060533 - 8 Jun 2019
Cited by 6 | Viewed by 3946
Abstract
Thirty-six female sheep, previously vaccinated against Bluetongue virus serotype 8 (BTV-8) using inactivated vaccines, were included in this field study. In Germany, vaccination was compulsory in 2008 and 2009, voluntary in 2010 and early 2011, and later, was prohibited in 2011. Due to [...] Read more.
Thirty-six female sheep, previously vaccinated against Bluetongue virus serotype 8 (BTV-8) using inactivated vaccines, were included in this field study. In Germany, vaccination was compulsory in 2008 and 2009, voluntary in 2010 and early 2011, and later, was prohibited in 2011. Due to their age, eighteen sheep had been vaccinated for two or more consecutive years, while a further eighteen animals had only been vaccinated once or not at all. The sheep were blood sampled five (n = 31) to 7.5 years (n = 5) after their last vaccination. All serum samples (n = 36) were tested for BTV group-specific antibodies by an ELISA (IDScreen® Bluetongue Competition assay, ID Vet). In five of the animals, the BTV-8 serotype-specific antibody titers were measured by serum neutralization (SN). The majority of sheep that were vaccinated annually for two or more years showed a positive ELISA (14/18 sheep) and a SN (two of two sheep) result 5 years after their last vaccination. Most of the sheep vaccinated fewer than twice showed a negative ELISA result 5 to 7.5 years after their last vaccination (13/18 animals). The three animals in this group tested by SN showed one negative and two positive results. This short communication is the first to describe the presence of BTV antibodies in sheep 5 to 7.5 years after vaccination with inactivated BTV-8 vaccines. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
22 pages, 8628 KiB  
Article
Attenuation of Bluetongue Virus (BTV) in an in ovo Model Is Related to the Changes of Viral Genetic Diversity of Cell-Culture Passaged BTV
by Fabian Z. X. Lean, Matthew J. Neave, John R. White, Jean Payne, Teresa Eastwood, Jemma Bergfeld, Antonio Di Rubbo, Vittoria Stevens, Kelly R. Davies, Joanne Devlin, David T. Williams and John Bingham
Viruses 2019, 11(5), 481; https://doi.org/10.3390/v11050481 - 26 May 2019
Cited by 6 | Viewed by 4665
Abstract
The embryonated chicken egg (ECE) is routinely used for the laboratory isolation and adaptation of Bluetongue virus (BTV) in vitro. However, its utility as an alternate animal model has not been fully explored. In this paper, we evaluated the pathogenesis of BTV in [...] Read more.
The embryonated chicken egg (ECE) is routinely used for the laboratory isolation and adaptation of Bluetongue virus (BTV) in vitro. However, its utility as an alternate animal model has not been fully explored. In this paper, we evaluated the pathogenesis of BTV in ovo using a pathogenic isolate of South African BTV serotype 3 (BTV-3) derived from the blood of an infected sheep. Endothelio- and neurotropism of BTV-3 were observed by immunohistochemistry of non-structural protein 1 (NS1), NS3, NS3/3a, and viral protein 7 (VP7) antigens. In comparing the pathogenicity of BTV from infectious sheep blood with cell-culture-passaged BTV, including virus propagated through a Culicoides-derived cell line (KC) or ECE, we found virus attenuation in ECE following cell-culture passage. Genomic analysis of the consensus sequences of segments (Seg)-2, -5, -6, -7, -8, -9, and -10 identified several nucleotide and amino-acid mutations among the cell-culture-propagated BTV-3. Deep sequencing analysis revealed changes in BTV-3 genetic diversity in various genome segments, notably a reduction of Seg-7 diversity following passage in cell culture. Using this novel approach to investigate BTV pathogenicity in ovo, our findings support the notion that pathogenic BTV becomes attenuated in cell culture and that this change is associated with virus quasispecies evolution. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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16 pages, 2478 KiB  
Article
Transcriptome Response of Female Culicoides sonorensis Biting Midges (Diptera: Ceratopogonidae) to Early Infection with Epizootic Hemorrhagic Disease Virus (EHDV-2)
by Dana Nayduch, Vijay Shankar, Mary K. Mills, Tanner Robl, Barbara S. Drolet, Mark G. Ruder, Erin D. Scully and Christopher A. Saski
Viruses 2019, 11(5), 473; https://doi.org/10.3390/v11050473 - 24 May 2019
Cited by 5 | Viewed by 4093
Abstract
Female Culicoides sonorensis biting midges are vectors of epizootic hemorrhagic disease virus (EHDV), which causes morbidity and mortality in wild and domesticated ruminants. The aims in this study were to identify key changes in female midge transcriptome profiles occurring during early infection with [...] Read more.
Female Culicoides sonorensis biting midges are vectors of epizootic hemorrhagic disease virus (EHDV), which causes morbidity and mortality in wild and domesticated ruminants. The aims in this study were to identify key changes in female midge transcriptome profiles occurring during early infection with EHDV-2. Midges were fed either negative control bloodmeals or bloodmeals containing EHDV-2 and transcriptomes were acquired at 36 h through deep sequencing. Reads were de novo assembled into a transcriptome comprised of 18,754 unigenes. Overall, there were 2401 differentially expressed unigenes and ~60% were downregulated in response to the virus (953 up; 1448 down). Downstream Gene Ontology enrichment, KEGG pathway mapping, and manual analyses were used to identify the effect of virus ingestion at both the gene and pathway levels. Downregulated unigenes were predominantly assigned to pathways related to cell/tissue structure and integrity (actin cytoskeleton, adherens junction, focal adhesion, hippo signaling), calcium signaling, eye morphogenesis and axon guidance. Unigenes attributed to sensory functions (especially vision), behavior, learning and memory were largely downregulated. Upregulated unigenes included those coding for innate immune processes, olfaction and photoreceptor pigments. Our results suggest that midges respond to virus infection as soon as 36 h post-ingestion, and that EHDV-2 may have a significant phenotypic effect on sensory and neural tissues. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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18 pages, 2001 KiB  
Article
Post-Epidemic Distribution of Schmallenberg Virus in Culicoides Arbovirus Vectors in Poland
by Julia Kęsik-Maliszewska, Magdalena Larska, Áine B. Collins and Jerzy Rola
Viruses 2019, 11(5), 447; https://doi.org/10.3390/v11050447 - 16 May 2019
Cited by 11 | Viewed by 2873
Abstract
Pooled samples of female and male Culicoides midges (5146 and 332 pools, respectively) that corresponded to a total number of 124,957 specimens were collected between 2013–2017 in the vicinity of cattle barns that were distributed throughout Poland were analyzed for the presence of [...] Read more.
Pooled samples of female and male Culicoides midges (5146 and 332 pools, respectively) that corresponded to a total number of 124,957 specimens were collected between 2013–2017 in the vicinity of cattle barns that were distributed throughout Poland were analyzed for the presence of Schmallenberg virus (SBV) RNA. Sixty-six pools tested positive (1.2%) with mean Ct value of 34.95. The maximum likelihood estimated infection rate (MLE) was calculated at 0.53 per 1000 individuals; however, it peaked in 2016 with MLE of 3.7. Viral RNA was detected in C. obsoletus/scoticus complex, C. punctatus, and C. pulicaris pools. Moreover, viral material was present in nulliparous (virgin) Culicoides females (MLE 0.27) and for the first time reported in males (MLE 0.34), which suggests the possibility of transovarial route of SBV or virus RNA transmission, as both do not fed on host blood. The accuracy of targeted versus random SBV surveillance in Culicoides vectors was compared. The relationship between infection rate (expressed as minimum infection rate; MIR), in addition to MLE, was compared with the density of virus infected midges (DIM). In conclusion, the SBV infection rate in the vector was significantly higher in 2016 as compared to other surveillance years; this is consistent with the simultaneous increase in SBV seroprevalence (seroconversion) in ruminants during the same year. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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13 pages, 1037 KiB  
Article
Phylogenetic Characterization of the Palyam Serogroup Orbiviruses
by Karen Ebersohn, Peter Coetzee, Louwrens P. Snyman, Robert Swanepoel and Estelle H. Venter
Viruses 2019, 11(5), 446; https://doi.org/10.3390/v11050446 - 16 May 2019
Cited by 10 | Viewed by 3102
Abstract
The Palyam serogroup orbiviruses are associated with abortion and teratogenesis in cattle and other ruminants. Of the 13 different serotypes that have been identified, the full genome sequence of only one, Kasba, has been published. We undertook to perform Next Generation Sequencing (NGS) [...] Read more.
The Palyam serogroup orbiviruses are associated with abortion and teratogenesis in cattle and other ruminants. Of the 13 different serotypes that have been identified, the full genome sequence of only one, Kasba, has been published. We undertook to perform Next Generation Sequencing (NGS) and phylogenetic analysis on 12 Palyam serotypes plus field isolates of the African serotypes in our possession. The Palyam serogroup was found to be most closely related to the African horse sickness virus group and showed the most distant evolutionary relationship to the equine encephalosis viruses (EEV). Amino acid sequence analysis revealed that the gene encoding VP7 was the most conserved within serotypes and VP2 and VP5 showed the highest degree of variation. A high degree of sequence identity was found for isolates from the same geographical region. The phylogenetic analysis revealed two clades where the African serotypes were all very closely related in one clade and the other clade contained the Australian and Asian serotypes and one African serotype, Petevo. It was evident from the sequence data that the geographical origin of Palyam serogroup viruses played an important role in the development of the different serotypes. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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15 pages, 1110 KiB  
Article
EHDV-2 Infection Prevalence Varies in Culicoides sonorensis after Feeding on Infected White-Tailed Deer over the Course of Viremia
by Sandra Y. Mendiola, Mary K. Mills, Elin Maki, Barbara S. Drolet, William C. Wilson, Roy Berghaus, David E. Stallknecht, Jonathan Breitenbach, D. Scott McVey and Mark G. Ruder
Viruses 2019, 11(4), 371; https://doi.org/10.3390/v11040371 - 23 Apr 2019
Cited by 13 | Viewed by 5272
Abstract
Epizootic hemorrhagic disease viruses (EHDVs) are arboviral pathogens of white-tailed deer and other wild and domestic ruminants in North America. Transmitted by various species of Culicoides, EHDVs circulate wherever competent vectors and susceptible ruminant host populations co-exist. The impact of variation in [...] Read more.
Epizootic hemorrhagic disease viruses (EHDVs) are arboviral pathogens of white-tailed deer and other wild and domestic ruminants in North America. Transmitted by various species of Culicoides, EHDVs circulate wherever competent vectors and susceptible ruminant host populations co-exist. The impact of variation in the level and duration of EHDV viremia in white-tailed deer (Odocoileus virginianus) on Culicoides infection prevalence is not well characterized. Here we examined how infection prevalence in a confirmed North American vector of EHDV-2 (Culicoides sonorensis) varies in response to fluctuations in deer viremia. To accomplish this, five white-tailed deer were experimentally infected with EHDV-2 and colonized C. sonorensis were allowed to feed on deer at 3, 5, 7, 10, 12, 14, 18, and 24 days post infection (dpi). Viremia profiles in deer were determined by virus isolation and titration at the same time points. Blood-fed Culicoides were assayed for virus after a 10-day incubation (27 °C) period. We found that increases in deer EHDV blood titers significantly increased both the likelihood that midges would successfully acquire EHDV and the proportion of midges that reached the titer threshold for transmission competence. Unexpectedly, we identified four infected midge samples (three individuals and one pool) after feeding on one deer 18 and 24 dpi, when viremia was no longer detectable by virus isolation. The ability of ruminants with low-titer viremia to serve as a source of EHDV for blood-feeding Culicoides should be explored further to better understand its potential epidemiological significance. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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15 pages, 1069 KiB  
Article
Vector Competence of Culicoides sonorensis (Diptera: Ceratopogonidae) for Epizootic Hemorrhagic Disease Virus Serotype 2 Strains from Canada and Florida
by Bethany L. McGregor, Dinesh Erram, Carolina Acevedo, Barry W. Alto and Nathan D. Burkett-Cadena
Viruses 2019, 11(4), 367; https://doi.org/10.3390/v11040367 - 22 Apr 2019
Cited by 10 | Viewed by 4005
Abstract
Epizootic hemorrhagic disease virus (EHDV), an Orbivirus transmitted by Culicoides spp. vectors, is represented by seven serotypes and numerous strains worldwide. While studies comparing vector competence between serotypes exist, studies between viral strains are lacking. In this study, we examined the rates of [...] Read more.
Epizootic hemorrhagic disease virus (EHDV), an Orbivirus transmitted by Culicoides spp. vectors, is represented by seven serotypes and numerous strains worldwide. While studies comparing vector competence between serotypes exist, studies between viral strains are lacking. In this study, we examined the rates of infection, dissemination, and transmission of two strains of EHDV-2 orally fed to the known vector, Culicoides sonorensis Wirth & Jones. Culicoides sonorensis cohorts were fed an infectious blood meal containing EHDV-2 strains from either Alberta, Canada (Can-Alberta) or Florida (5.5 log10 PFUe/mL) and tested for the vector’s susceptibility to infection and dissemination. In addition, transmission rates of the virus were assessed and compared using capillary tube and honey card methods. Our results show that the Florida strain had higher infection and dissemination rates than the Can-Alberta strain in spite of the Florida strain having significantly lower viral titers in C. sonorensis bodies, legs, and saliva than the Can-Alberta strain. Overall transmission rates were not significantly different between the two strains but varied significantly between the methods used. These findings suggest that the consequences of EHDV infection in C. sonorensis vary between virus strains and have huge implications in future vector competence studies involving Culicoides species and Orbiviruses. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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Review

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11 pages, 482 KiB  
Review
Schmallenberg Disease—A Newly Emerged Culicoides-Borne Viral Disease of Ruminants
by Abaineh D. Endalew, Bonto Faburay, William C. Wilson and Juergen A. Richt
Viruses 2019, 11(11), 1065; https://doi.org/10.3390/v11111065 - 15 Nov 2019
Cited by 24 | Viewed by 5531
Abstract
First appearing in 2011 in Northern Europe, Schmallenberg virus (SBV), an Orthobunyavirus of the Simbu serogroup, is associated with clinical disease mainly in ruminants such as cattle, sheep and goats. The clinical signs are characterized by abortion and congenital deformities in newborns. The [...] Read more.
First appearing in 2011 in Northern Europe, Schmallenberg virus (SBV), an Orthobunyavirus of the Simbu serogroup, is associated with clinical disease mainly in ruminants such as cattle, sheep and goats. The clinical signs are characterized by abortion and congenital deformities in newborns. The virus is transmitted by Culicoides midges of the Obsoletus complex. SBV infection induces a solid protective immunity that persists for at least 4 or 6 years in sheep and cattle, respectively. SBV infection can be diagnosed directly by real-time RT-qPCR and virus isolation or indirectly by serological assays. Three vaccines are commercially available in Europe. This article provides a comprehensive literature review on this emerging disease regarding pathogenesis, transmission, diagnosis, control and prevention. This review also highlights that although much has been learned since SBV’s first emergence, there are still areas that require further study to devise better mitigation strategies. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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19 pages, 645 KiB  
Review
Reliable and Standardized Animal Models to Study the Pathogenesis of Bluetongue and Schmallenberg Viruses in Ruminant Natural Host Species with Special Emphasis on Placental Crossing
by Ludovic Martinelle, Fabiana Dal Pozzo, Etienne Thiry, Kris De Clercq and Claude Saegerman
Viruses 2019, 11(8), 753; https://doi.org/10.3390/v11080753 - 15 Aug 2019
Cited by 6 | Viewed by 4023
Abstract
Starting in 2006, bluetongue virus serotype 8 (BTV8) was responsible for a major epizootic in Western and Northern Europe. The magnitude and spread of the disease were surprisingly high and the control of BTV improved significantly with the marketing of BTV8 inactivated vaccines [...] Read more.
Starting in 2006, bluetongue virus serotype 8 (BTV8) was responsible for a major epizootic in Western and Northern Europe. The magnitude and spread of the disease were surprisingly high and the control of BTV improved significantly with the marketing of BTV8 inactivated vaccines in 2008. During late summer of 2011, a first cluster of reduced milk yield, fever, and diarrhoea was reported in the Netherlands. Congenital malformations appeared in March 2012 and Schmallenberg virus (SBV) was identified, becoming one of the very few orthobunyaviruses distributed in Europe. At the start of both epizootics, little was known about the pathogenesis and epidemiology of these viruses in the European context and most assumptions were extrapolated based on other related viruses and/or other regions of the World. Standardized and repeatable models potentially mimicking clinical signs observed in the field are required to study the pathogenesis of these infections, and to clarify their ability to cross the placental barrier. This review presents some of the latest experimental designs for infectious disease challenges with BTV or SBV. Infectious doses, routes of infection, inoculum preparation, and origin are discussed. Particular emphasis is given to the placental crossing associated with these two viruses. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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13 pages, 719 KiB  
Review
Bluetongue Virus in France: An Illustration of the European and Mediterranean Context since the 2000s
by Cindy Kundlacz, Grégory Caignard, Corinne Sailleau, Cyril Viarouge, Lydie Postic, Damien Vitour, Stéphan Zientara and Emmanuel Breard
Viruses 2019, 11(7), 672; https://doi.org/10.3390/v11070672 - 23 Jul 2019
Cited by 28 | Viewed by 5770
Abstract
Bluetongue (BT) is a non-contagious animal disease transmitted by midges of the Culicoides genus. The etiological agent is the BT virus (BTV) that induces a variety of clinical signs in wild or domestic ruminants. BT is included in the notifiable diseases list of [...] Read more.
Bluetongue (BT) is a non-contagious animal disease transmitted by midges of the Culicoides genus. The etiological agent is the BT virus (BTV) that induces a variety of clinical signs in wild or domestic ruminants. BT is included in the notifiable diseases list of the World Organization for Animal Health (OIE) due to its health impact on domestic ruminants. A total of 27 BTV serotypes have been described and additional serotypes have recently been identified. Since the 2000s, the distribution of BTV has changed in Europe and in the Mediterranean Basin, with continuous BTV incursions involving various BTV serotypes and strains. These BTV strains, depending on their origin, have emerged and spread through various routes in the Mediterranean Basin and/or in Europe. Consequently, control measures have been put in place in France to eradicate the virus or circumscribe its spread. These measures mainly consist of assessing virus movements and the vaccination of domestic ruminants. Many vaccination campaigns were first carried out in Europe using attenuated vaccines and, in a second period, using exclusively inactivated vaccines. This review focuses on the history of the various BTV strain incursions in France since the 2000s, describing strain characteristics, their origins, and the different routes of spread in Europe and/or in the Mediterranean Basin. The control measures implemented to address this disease are also discussed. Finally, we explain the circumstances leading to the change in the BTV status of France from BTV-free in 2000 to an enzootic status since 2018. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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12 pages, 701 KiB  
Review
Bovine Ephemeral Fever in Asia: Recent Status and Research Gaps
by Fan Lee
Viruses 2019, 11(5), 412; https://doi.org/10.3390/v11050412 - 3 May 2019
Cited by 33 | Viewed by 6673
Abstract
Bovine ephemeral fever is an arthropod-borne viral disease affecting mainly domestic cattle and water buffalo. The etiological agent of this disease is bovine ephemeral fever virus, a member of the genus Ephemerovirus within the family Rhabdoviridae. Bovine ephemeral fever causes economic losses [...] Read more.
Bovine ephemeral fever is an arthropod-borne viral disease affecting mainly domestic cattle and water buffalo. The etiological agent of this disease is bovine ephemeral fever virus, a member of the genus Ephemerovirus within the family Rhabdoviridae. Bovine ephemeral fever causes economic losses by a sudden drop in milk production in dairy cattle and loss of condition in beef cattle. Although mortality resulting from this disease is usually lower than 1%, it can reach 20% or even higher. Bovine ephemeral fever is distributed across many countries in Asia, Australia, the Middle East, and Africa. Prevention and control of the disease mainly relies on regular vaccination. The impact of bovine ephemeral fever on the cattle industry may be underestimated, and the introduction of bovine ephemeral fever into European countries is possible, similar to the spread of bluetongue virus and Schmallenberg virus. Research on bovine ephemeral fever remains limited and priority of investigation should be given to defining the biological vectors of this disease and identifying virulence determinants. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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19 pages, 558 KiB  
Review
Culicoides Biting Midges—Underestimated Vectors for Arboviruses of Public Health and Veterinary Importance
by Franziska Sick, Martin Beer, Helge Kampen and Kerstin Wernike
Viruses 2019, 11(4), 376; https://doi.org/10.3390/v11040376 - 24 Apr 2019
Cited by 79 | Viewed by 8329
Abstract
Culicoides biting midges, small hematophagous dipterans, are the demonstrated or putative vectors of multiple arboviruses of veterinary and public health importance. Despite its relevance in disease spread, the ceratopogonid genus Culicoides is still a largely neglected group of species, predominantly because the major [...] Read more.
Culicoides biting midges, small hematophagous dipterans, are the demonstrated or putative vectors of multiple arboviruses of veterinary and public health importance. Despite its relevance in disease spread, the ceratopogonid genus Culicoides is still a largely neglected group of species, predominantly because the major human-affecting arboviruses are considered to be transmitted by mosquitoes. However, when a pathogen is detected in a certain vector species, a thorough search for further vectors often remains undone and, therefore, the relevant vector species may remain unknown. Furthermore, for many hematophagous arthropods, true vector competence is often merely suspected and not experimentally proven. Therefore, we aim to illuminate the general impact of Culicoides biting midges and to summarize the knowledge about biting midge-borne disease agents using the order Bunyavirales, the largest and most diverse group of RNA viruses, as an example. When considering only viruses evidentially transmitted by Culicoides midges, the Simbu serogroup (genus Orthobunyavirus) is presumably the most important group within the virus order. Its members are of great veterinary importance, as a variety of simbuviruses, e.g., the species Akabane orthobunyavirus or Schmallenberg orthobunyavirus, induces severe congenital infections in pregnant animals. The major zoonotic representative of this serogroup occurs in South and Central America and causes the so-called Oropouche fever, an acute febrile illness in humans. Full article
(This article belongs to the Special Issue Virus-Vector-Host Interactions of Culicoides-Borne Diseases)
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