Bluetongue, Epizootic Haemorrhagic Disease, and Other Emerging Orbiviruses

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

Deadline for manuscript submissions: closed (31 August 2024) | Viewed by 10273

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Istituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise G. Caporale, 64100 Teramo, Italy
Interests: arboviroses
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Istituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise G. Caporale, 64100 Teramo, Italy
Interests: arboviroses

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Food and Agriculture Organization (FAO), Rome, Italy
Interests: arboviroses

Special Issue Information

Dear Colleagues,

Orbivirus is the largest genus of the new named Sedoreoviridae family. It contains 22 species and more than 130 serotypes.  Most of the species that belong to this genus are arboviruses. Their biological transmission involves three essential actors: viruses, vectors, and vertebrates. Orbiviruses occur globally and infect a wide variety of arthropods and vertebrate hosts. Vectors include ticks, mosquitoes, sand flies, and biting midges; while vertebrate hosts include bats, birds, marsupials, rodents, sloths, equids, wild and domestic ruminants, human and non-human primates. Although some species like Lebombo and Orungo viruses are regarded as mild human pathogens, the importance of this genus is mostly associated with those species, which can cause severe diseases in livestock. Bluetongue (BTV), Epizootic Haemorrhagic disease (EHDV), and African horse sickness viruses (AHSV) are considered major animal pathogens. BTV, EHDV, and AHSV can seriously affect animal welfare and the international trade of livestock, producing severe economic losses to the livestock production and pastoral economy of the affected countries. Over the last decades, due to globalization and climate change, the distribution and activity of arthropod vectors have been exacerbated, facilitating the spread of arthropod-borne viruses in general, and of the Orbiviruses in particular. These new scenarios provided the basis for the occurrence of new emerging disease problems in many countries, as evidenced by recent incursions and outbreaks of BTV-3 and EHDV-8 in Europe.

The continual occurrence of new scenarios and evolution of the Orbivirus species pose a substantial challenge to the research community. Within this context, this Special Issue intends to collect reviews or original contributions from researchers involved in the multidisciplinary aspects that the interactions between viruses, hosts, and vectors inevitably imply. To this extent, contributions enlightening the epidemiology, pathogenesis, and diagnosis of these viruses are welcome, as well as those studies that provide further insights into the critical role played by control strategies and propose new and more efficacious control methods.

Dr. Giovanni Savini
Dr. Massimo Spedicato
Dr. Soufien Sghaier
Guest Editors

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Keywords

  • bluetongue virus
  • epizootic haemorragic disease
  • orbivirus
  • arbovirus
  • culicoides
  • vectors
  • climate
  • livestock
  • virus–host–vector interactions
  • pathogenesis
  • immunology
  • vaccines
  • diagnostics
  • epidemiology
  • cattle
  • sheep
  • goats
  • ruminants
  • wildlife animals
  • drivers
  • risk pathway
  • risk analysis
  • modelling
  • control
  • prevention
  • surveillance
  • economic impact
  • antiviral agents and related resistance

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Published Papers (8 papers)

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Research

17 pages, 3652 KiB  
Article
Immunological and Pathogenic Differences of Two Experimental Bluetongue Virus Serotype Infections Evaluated in Two Disparate Host Species
by Joseph A. Westrich, Erin E. McNulty, Madison Stoltz, Tyler J. Sherman, Molly Carpenter, Mollie Burton, Amy Nalls, Hennio S. Rubio, Audrey Sandoval, Christie Mayo and Candace K. Mathiason
Viruses 2024, 16(10), 1593; https://doi.org/10.3390/v16101593 - 10 Oct 2024
Viewed by 500
Abstract
Bluetongue virus (BTV) is a prevalent midge-borne pathogen that infects ruminant species worldwide. BTV infections range from asymptomatic to lethal, with mechanisms that determine the severity of infection remaining largely undefined. Although it is relatively poorly understood, the immune response to BTV infection [...] Read more.
Bluetongue virus (BTV) is a prevalent midge-borne pathogen that infects ruminant species worldwide. BTV infections range from asymptomatic to lethal, with mechanisms that determine the severity of infection remaining largely undefined. Although it is relatively poorly understood, the immune response to BTV infection is thought to be critical for both the propagation of disease as well as the resolution of infection. To bridge this gap in knowledge, we infected cohorts of sheep and muntjac deer with two serotypes of BTV (BTV10 and BTV17) for longitudinal analysis (30 days). Interestingly, species-specific differences were observed. Circulating virus was detected early and remained detectable for the duration of the sheep study, while infections in muntjac showed faltering detection of BTV10 at 3 weeks post infection. The magnitude of the immune response was subdued in the muntjac when compared to the sheep cohorts, though similar responses were observed. We also assessed midge viral uptake and the ability to replicate BTV. Midges successfully fed on both species, yet those that fed on sheep resulted in more efficient BTV transmission. Our findings demonstrate that differences in BTV infections, immune responses, and vector competence across host species and serotypes will impact global BTV emergence and strategies for mitigation. Full article
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16 pages, 3327 KiB  
Article
Increased Virulence of Culicoides Midge Cell-Derived Bluetongue Virus in IFNAR Mice
by Barbara S. Drolet, Lindsey Reister-Hendricks, Christie Mayo, Case Rodgers, David C. Molik and David Scott McVey
Viruses 2024, 16(9), 1474; https://doi.org/10.3390/v16091474 - 17 Sep 2024
Viewed by 824
Abstract
Bluetongue (BT) is a Culicoides midge-borne hemorrhagic disease affecting cervids and ruminant livestock species, resulting in significant economic losses from animal production and trade restrictions. Experimental animal infections using the α/β interferon receptor knockout IFNAR mouse model and susceptible target species are critical [...] Read more.
Bluetongue (BT) is a Culicoides midge-borne hemorrhagic disease affecting cervids and ruminant livestock species, resulting in significant economic losses from animal production and trade restrictions. Experimental animal infections using the α/β interferon receptor knockout IFNAR mouse model and susceptible target species are critical for understanding viral pathogenesis, virulence, and evaluating vaccines. However, conducting experimental vector-borne transmission studies with the vector itself are logistically difficult and experimentally problematic. Therefore, experimental infections are induced by hypodermic injection with virus typically derived from baby hamster kidney (BHK) cells. Unfortunately, for many U.S. BTV serotypes, it is difficult to replicate the severity of the disease seen in natural, midge-transmitted infections by injecting BHK-derived virus into target host animals. Using the IFNAR BTV murine model, we compared the virulence of traditional BHK cell-derived BTV-17 with C. sonorensis midge (W8) cell-derived BTV-17 to determine whether using cells of the transmission vector would provide an in vitro virulence aspect of vector-transmitted virus. At both low and high doses, mice inoculated with W8-BTV-17 had an earlier onset of viremia, earlier onset and peak of clinical signs, and significantly higher mortality compared to mice inoculated with BHK-BTV-17. Our results suggest using a Culicoides W8 cell-derived inoculum may provide an in vitro vector-enhanced infection to more closely represent disease levels seen in natural midge-transmitted infections while avoiding the logistical and experimental complexity of working with live midges. Full article
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17 pages, 1558 KiB  
Article
Modelling the Influence of Climate and Vector Control Interventions on Arbovirus Transmission
by Emma L. Fairbanks, Janet M. Daly and Michael J. Tildesley
Viruses 2024, 16(8), 1221; https://doi.org/10.3390/v16081221 - 30 Jul 2024
Viewed by 805
Abstract
Most mathematical models that assess the vectorial capacity of disease-transmitting insects typically focus on the influence of climatic factors to predict variations across different times and locations, or examine the impact of vector control interventions to forecast their potential effectiveness. We combine features [...] Read more.
Most mathematical models that assess the vectorial capacity of disease-transmitting insects typically focus on the influence of climatic factors to predict variations across different times and locations, or examine the impact of vector control interventions to forecast their potential effectiveness. We combine features of existing models to develop a novel model for vectorial capacity that considers both climate and vector control. This model considers how vector control tools affect vectors at each stage of their feeding cycle, and incorporates host availability and preference. Applying this model to arboviruses of veterinary importance in Europe, we show that African horse sickness virus (AHSV) has a higher peak predicted vectorial capacity than bluetongue virus (BTV), Schmallenberg virus (SBV), and epizootic haemorrhagic disease virus (EHDV). However, AHSV has a shorter average infectious period due to high mortality; therefore, the overall basic reproduction number of AHSV is similar to BTV. A comparable relationship exists between SBV and EHDV, with both viruses showing similar basic reproduction numbers. Focusing on AHSV transmission in the UK, insecticide-treated stable netting is shown to significantly reduce vectorial capacity of Culicoides, even at low coverage levels. However, untreated stable netting is likely to have limited impact. Overall, this model can be used to consider both climate and vector control interventions either currently utilised or for potential use in an outbreak, and could help guide policy makers seeking to mitigate the impact of climate change on disease control. Full article
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13 pages, 2124 KiB  
Article
Reference Material Production and Milk Protein Concentration as Elements to Improve Bluetongue Serological Diagnosis in Bulk Tank Milk
by David Romero-Trancón, Marta Valero-Lorenzo, Montserrat Agüero and Rubén Villalba
Viruses 2024, 16(6), 915; https://doi.org/10.3390/v16060915 - 4 Jun 2024
Viewed by 938
Abstract
The serological surveillance of bluetongue in bulk tank milk is an efficient and cost-effective method for the early detection of bluetongue virus incursions in unvaccinated free areas of the disease. In addition, the availability of standardized and reliable reagents and refined diagnostic procedures [...] Read more.
The serological surveillance of bluetongue in bulk tank milk is an efficient and cost-effective method for the early detection of bluetongue virus incursions in unvaccinated free areas of the disease. In addition, the availability of standardized and reliable reagents and refined diagnostic procedures with high sensitivity and specificity are essential for surveillance purposes. However, no available reference materials for bluetongue virus serological surveillance in bulk tank milk exist. This study shows the production and characterization of reference material for the implementation of a commercially available bluetongue milk ELISA test in official laboratories, as well as the evaluation of a procedure to increase the sensitivity in samples with low levels of antibodies. This procedure, based on milk protein concentration, allowed us to notably increase the ELISA test’s analytical sensitivity, which is useful for milk samples from farms with low within-herd prevalence or pools of bulk tank milk samples. The standardized milk reference material produced here, together with the evaluated procedure to improve analytical sensitivity, could be applied as tools to ensure an accurate diagnosis by official laboratories in bluetongue unvaccinated free areas. Full article
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20 pages, 3971 KiB  
Article
Culicoides Midge Abundance across Years: Modeling Inter-Annual Variation for an Avian Feeder and a Candidate Vector of Hemorrhagic Diseases in Farmed Wildlife
by Jamie S. Benn, Jeremy P. Orange, Juan Pablo Gomez, Emily T. N. Dinh, Bethany L. McGregor, Erik M. Blosser, Nathan D. Burkett-Cadena, Samantha M. Wisely and Jason K. Blackburn
Viruses 2024, 16(5), 766; https://doi.org/10.3390/v16050766 - 11 May 2024
Viewed by 1151
Abstract
(1) Background: Epizootic hemorrhagic disease virus (EHDV) and bluetongue virus (BTV) are orbiviruses that cause hemorrhagic disease (HD) with significant economic and population health impacts on domestic livestock and wildlife. In the United States, white-tailed deer (Odocoileus virginianus) are particularly susceptible [...] Read more.
(1) Background: Epizootic hemorrhagic disease virus (EHDV) and bluetongue virus (BTV) are orbiviruses that cause hemorrhagic disease (HD) with significant economic and population health impacts on domestic livestock and wildlife. In the United States, white-tailed deer (Odocoileus virginianus) are particularly susceptible to these viruses and are a frequent blood meal host for various species of Culicoides biting midges (Diptera: Ceratopogonidae) that transmit orbiviruses. The species of Culicoides that transmit EHDV and BTV vary between regions, and larval habitats can differ widely between vector species. Understanding how midges are distributed across landscapes can inform HD virus transmission risk on a local scale, allowing for improved animal management plans to avoid suspected high-risk areas or target these areas for insecticide control. (2) Methods: We used occupancy modeling to estimate the abundance of gravid (egg-laden) and parous (most likely to transmit the virus) females of two putative vector species, C. stellifer and C. venustus, and one species, C. haematopotus, that was not considered a putative vector. We developed a universal model to determine habitat preferences, then mapped a predicted weekly midge abundance during the HD transmission seasons in 2015 (July–October) and 2016 (May–October) in Florida. (3) Results: We found differences in habitat preferences and spatial distribution between the parous and gravid states for C. haematopotus and C. stellifer. Gravid midges preferred areas close to water on the border of well and poorly drained soil. They also preferred mixed bottomland hardwood habitats, whereas parous midges appeared less selective of habitat. (4) Conclusions: If C. stellifer is confirmed as an EHDV vector in this region, the distinct spatial and abundance patterns between species and physiological states suggest that the HD risk is non-random across the study area. Full article
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10 pages, 1728 KiB  
Article
Spatial Transmission Characteristics of the Bluetongue Virus Serotype 3 Epidemic in The Netherlands, 2023
by Gert-Jan Boender, Thomas J. Hagenaars, Melle Holwerda, Marcel A. H. Spierenburg, Piet A. van Rijn, Arco N. van der Spek and Armin R. W. Elbers
Viruses 2024, 16(4), 625; https://doi.org/10.3390/v16040625 - 17 Apr 2024
Cited by 3 | Viewed by 1914
Abstract
A devastating bluetongue (BT) epidemic caused by bluetongue virus serotype 3 (BTV-3) has spread throughout most of the Netherlands within two months since the first infection was officially confirmed in the beginning of September 2023. The epidemic comes with unusually strong suffering of [...] Read more.
A devastating bluetongue (BT) epidemic caused by bluetongue virus serotype 3 (BTV-3) has spread throughout most of the Netherlands within two months since the first infection was officially confirmed in the beginning of September 2023. The epidemic comes with unusually strong suffering of infected cattle through severe lameness, often resulting in mortality or euthanisation for welfare reasons. In total, tens of thousands of sheep have died or had to be euthanised. By October 2023, more than 2200 locations with ruminant livestock were officially identified to be infected with BTV-3, and additionally, ruminants from 1300 locations were showing BTV-associated clinical symptoms (but not laboratory-confirmed BT). Here, we report on the spatial spread and dynamics of this BT epidemic. More specifically, we characterized the distance-dependent intensity of the between-holding transmission by estimating the spatial transmission kernel and by comparing it to transmission kernels estimated earlier for BTV-8 transmission in Northwestern Europe in 2006 and 2007. The 2023 BTV-3 kernel parameters are in line with those of the transmission kernel estimated previously for the between-holding spread of BTV-8 in Europe in 2007. The 2023 BTV-3 transmission kernel has a long-distance spatial range (across tens of kilometres), evidencing that in addition to short-distance dispersal of infected midges, other transmission routes such as livestock transports probably played an important role. Full article
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12 pages, 671 KiB  
Article
Development and Validation of Three Triplex Real-Time RT-PCR Assays for Typing African Horse Sickness Virus: Utility for Disease Control and Other Laboratory Applications
by Rubén Villalba, Cristina Tena-Tomás, María José Ruano, Marta Valero-Lorenzo, Ana López-Herranz, Cristina Cano-Gómez and Montserrat Agüero
Viruses 2024, 16(3), 470; https://doi.org/10.3390/v16030470 - 20 Mar 2024
Cited by 1 | Viewed by 1267
Abstract
The African horse sickness virus (AHSV) belongs to the Genus Orbivirus, family Sedoreoviridae, and nine serotypes of the virus have been described to date. The AHSV genome is composed of ten linear segments of double-stranded (ds) RNA, numbered in decreasing size order (Seg-1 [...] Read more.
The African horse sickness virus (AHSV) belongs to the Genus Orbivirus, family Sedoreoviridae, and nine serotypes of the virus have been described to date. The AHSV genome is composed of ten linear segments of double-stranded (ds) RNA, numbered in decreasing size order (Seg-1 to Seg-10). Genome segment 2 (Seg-2) encodes outer-capsid protein VP2, the most variable AHSV protein and the primary target for neutralizing antibodies. Consequently, Seg-2 determines the identity of the virus serotype. An African horse sickness (AHS) outbreak in an AHS-free status country requires identifying the serotype as soon as possible to implement a serotype-specific vaccination program. Considering that nowadays ‘polyvalent live attenuated’ is the only commercially available vaccination strategy to control the disease, field and vaccine strains of different serotypes could co-circulate. Additionally, in AHS-endemic countries, more than one serotype is often circulating at the same time. Therefore, a strategy to rapidly determine the virus serotype in an AHS-positive sample is strongly recommended in both epidemiological situations. The main objective of this study is to describe the development and validation of three triplex real-time RT-PCR (rRT-PCR) methods for rapid AHSV serotype detection. Samples from recent AHS outbreaks in Kenia (2015–2017), Thailand (2020), and Nigeria (2023), and from the AHS outbreak in Spain (1987–1990), were included in the study for the validation of these methods. Full article
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13 pages, 3565 KiB  
Article
Epidemiological Analyses of the First Incursion of the Epizootic Hemorrhagic Disease Virus Serotype 8 in Tunisia, 2021–2022
by Thameur Ben Hassine, José-María García-Carrasco, Soufien Sghaier, Sarah Thabet, Alessio Lorusso, Giovanni Savini and Salah Hammami
Viruses 2024, 16(3), 362; https://doi.org/10.3390/v16030362 - 27 Feb 2024
Cited by 1 | Viewed by 2027
Abstract
Epizootic hemorrhagic disease (EHD) is a non-contagious arthropod-transmitted viral disease and a World Organization for Animal Health (WOAH)-listed disease of domestic and wild ruminants since 2008. EHDV is transmitted among susceptible animals by a few species of midges of genus Culicoides. During [...] Read more.
Epizootic hemorrhagic disease (EHD) is a non-contagious arthropod-transmitted viral disease and a World Organization for Animal Health (WOAH)-listed disease of domestic and wild ruminants since 2008. EHDV is transmitted among susceptible animals by a few species of midges of genus Culicoides. During the fall of 2021, a large outbreak caused by the epizootic hemorrhagic disease virus (EHDV), identified as serotype 8, was reported in Tunisian dairy and beef farms with Bluetongue virus (BTV)-like clinical signs. The disease was detected later in the south of Italy, in Spain, in Portugal and, more recently, in France, where it caused severe infections in cattle. This was the first evidence of EHDV-8 circulation outside Australia since 1982. In this study, we analyzed the epidemiological situation of the 2021–2022 EHDV outbreaks reported in Tunisia, providing a detailed description of the spatiotemporal evolution of the disease. We attempted to identify the eco-climatic factors associated with infected areas using generalized linear models (GLMs). Our results demonstrated that environmental factors mostly associated with the presence of C. imicola, such as digital elevation model (DEM), slope, normalized difference vegetation index (NDVI), and night-time land surface temperature (NLST)) were by far the most explanatory variables for EHD repartition cases in Tunisia that may have consequences in neighboring countries, both in Africa and Europe through the spread of infected vectors. The risk maps elaborated could be useful for disease control and prevention strategies. Full article
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