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Schmallenberg virus: State of Art

EFSA Journal 2014;12(5):3681 [54 pp.]. doi:10.2903/j.efsa.2014.3681
European Food Safety Authority Acknowledgment EFSA wishes to thank the members of the Working Group on Schmallenberg Mandate II: Thomas Balenghien, Simon Gubbins, Anthony Wilson, Matthew Baylis, Richard Elliott, Stefan Zientara, Antoine Poskin, Claire Ponsart and Brigitte Cay and EFSA staff: José Cortiñas Abrahantes, Anna Zuliani, Ana Afonso, Jane Richardson, Andrea Bau, Franck Berthe and Didier Verloo for the support provided to this scientific output and Arjan Stegeman for peer reviewing the publication. Contact amu@efsa.europa.eu
Type: Scientific Report of EFSA On request from: European Commission Question number: EFSA-Q-2012-00824 Approved: 30 April 2014 Published: 15 May 2014 Affiliation: European Food Safety Authority (EFSA) Parma Italy
Abstract

This scientific report provides an overview of all research carried out on Schmallenberg virus (SBV), reviewing the current knowledge on SBV regarding genotyping findings, susceptible species, pathogenesis, transmission routes, immunity, seroprevalence, geographical and temporal SBV spread, improved within-herd transmission model, SBV impact assessment and within-herd and regional spread models. Metagenomic analysis identified SBV as a novel orthobunyavirus emerged in 2011 and it has been detected in domestic cattle, sheep, goats and 12 wild species. Seroprevalence studies indicate that SBV has probably spread over the whole of Europe, showing high seroprevalence at national scale, while larger variability is observed at regional scales. Clinical disease frequency is low and experimental infection on pregnant ewes and cows suggest that SBV rarely induces malformations. SBV may be detected from semen with a low frequency though there is no scientific evidence of transmission through insemination. Vector competence studies suggest that Culicoides are likely to be able to transmit SBV but found no evidence that mosquitoes are likely to be able to transmit it. SBV vertical transmission has not yet been identified as a major route. SBV has successfully overwintered, despite lengthy period of minimal vector activity and duration of immunity in cattle lasts for at least one year. A farm-to-farm spread model for SBV shows a rapid spread of infection across the study region and latent period, duration of viraemia, probability of transmission from host to vector and virus replication are sufficient to account for the rapid SBV spread. The between-farm SBV transmission model indicates that the application of movement restrictions has little effect on SBV spread. An impact assessment based on limited data suggests a probable effect of SBV infection on abortion, short gestation, non-return and the number of artificial inseminations required per animal. International trade restrictions by third countries represent the main SBV impact.

© European Food Safety Authority, 2014

Summary

This scientific report provides an overview of research carried out on Schmallenberg virus in the different Member States (MS), with special attention given to research co-financed by the European Commission, focusing in particular on three main research lines:

  • A review of the current knowledge of SBV regarding:
    • Genetic analysis findings
    • Susceptible species reported
    • Pathogenesis, covering viraemic and susceptible periods
    • Potential transmission routes, discussing horizontal, vertical and vector-borne transmission as well as the ability of each to explain overwintering
    • Duration of immunity
    • Findings from seroprevalence studies conducted in different MS.
  • The use of transmission models to evaluate geographical as well as temporal spread of SBV, specifically:
    • a within-farm transmission model using the large scale seroprevalence studies from Belgium and the Netherlands to estimate within-herd transmission parameters
    • a network model describing regional spread and the potential impact of animal movement restrictions SBV spread
    • A modified continental spread model similar to that presented in the previous scientific report but exploring a broader range of possible transmission kernels.
  • Summarizing SBV impact assessment carried out in several MS.

Metagenomic analysis of animal material allowed the rapid identification of SBV, a newly discovered orthobunyavirus related to viruses in the Simbu serogroup, as the cause of the new disease that emerged in 2011. The availability of the (almost) complete nucleotide sequence of the SBV genome enabled a PCR test for SBV to be developed and distributed throughout Europe. It also contributes to the establishment of reverse genetic systems (Elliott et. al., 2013; Varela et. al., 2013) that will facilitate further research on SBV molecular biology, pathogenesis and vaccine development. The genome sequencing also highlighted the need for wide-scale sequencing studies on orthobunyaviruses in general as this would have helped to more quickly understand the relationship between SBV and extant Simbu serogroup viruses as well as the origin of SBV.

SBV RNA or antibodies have been detected in domestic cattle, sheep and goats and also in another 12 wild species: Alpacas, Anatolian water buffalo, Elk, Bison, Red deer, Fallow deer, Roe deer, Sika deer, Muntjac, Chamois, Wild boar and Dogs, as well as in 19 zoo species. The seroprevalence studies in cattle, sheep and goats indicate that SBV has probably spread over the whole of Europe. According to the seroprevalence studies conducted at national scale, prevalence at animal and herd levels were in general high, while for the regional studies a larger variability was observed.

The number of herds with SBV confirmed AHS (arthrogryposis hydranencephaly syndrome) cases compared to the level of infection indicated by seroprevalence studies, suggest that the frequency of clinical disease is low. SBV induces malformed calves only in a very limited number of cases, as demonstrated by experimental infection studies on pregnant cows and ewes. Although these resulted in only one malformed calf out of a total of 24 foetuses from a cow inoculated at day 90 of pregnancy, the presence of viral RNA could be demonstrated in the placenta of some ewes. The proportion of positive placenta and foetuses was higher in the group of ewes infected at day 45 of pregnancy compared to the ewes infected at day 38 of pregnancy in one experiment and at day 60 compared to day 45 in the other experiment. From these studies it can be concluded that SBV infection leads only in a very limited number of cases to malformation even when the experimental infection is performed during the susceptible period.

Limited numbers of articles have studied the risks of transmission of these viruses via semen and embryos. Recent data indicate that SBV may be detected in semen samples with a low frequency (<6 %). However, there is no scientific evidence of transmission through insemination. This is in agreement with epidemiological data, indicating that the vector transmission remains the principal route explaining the dissemination of such viruses. Details are given below.

Phylogenetic relations of SBV with viruses of the Simbu serogroup led to suspicion that SBV was transmitted by Culicoides. Following detection of the SBV incursion, vector competence assays were performed on colonized mosquitoes and both colonized and field collected Culicoides (Veronesi et. al., 2013b; Balenghien et. al., 2014). These studies confirmed that several Culicoides species are likely to be capable of transmitting SBV but provided no evidence that the mosquito species studied are likely to be able to act as vectors. Viral RNA presence was also assessed in field collected Culicoides from farms in the affected regions. Studies in Belgium, Netherlands and France (De Regge et. al., 2012; Elbers et. al., 2013a; Balenghien et. al., 2014) also suggest a high probability that C. obsoletus, C. scoticus and C. chiopterus have a role as vectors of SBV in northern Europe. C. dewulfi, C. pulicaris, C. nubeculosus and C. punctatus have also been implicated as suspected vectors in Belgium, France or Poland (De Regge et. al., 2012; Larska et. al., 2013; Balenghien et. al., 2014), although quantities of SBV RNA detected were equivocal in defining the level of dissemination that had occurred (Veronesi et. al., 2013b). Studies of C. imicola in Sardinia failed to convincingly implicate this species in SBV transmission (Balenghien et. al., 2014). Vector competence studies currently being conducted in Italy will indicate the competence of C. imicola for SBV. Taken in their entirety, these studies convincingly implicated a range of widespread and abundant farm-associated Culicoides species in the transmission of SBV, including at least the species C. obsoletus, C. scoticus and C. chiopterus.

There is no evidence yet that vertical transmission is a major route of transmission of SBV. SBV has been detected in certain tissues of clinically-affected newborn calves, kids and lambs but neither SBV virus nor RNA has been documented in their blood. There is therefore currently no evidence to suggest that clinically affected newborns represent a viable source of virus for vectors. There is limited evidence for the transmission of SBV to progeny Culicoides.

SBV has successfully overwintered, despite lengthy period of minimal vector activity. The mechanism is unknown at present; however vertical transmission in host or vector may play a role. Evidence of persistent infection in the host has not been yet documented.

There are only limited data on duration of immunity in cattle and none on the duration of immunity in sheep. The data for cattle suggest that immunity lasts for at least one year following natural infection. Data on immunity over longer periods is not yet available.

A model for the farm to farm spread of a vector-borne virus parameterized for SBV show a rapid spread of infection across the study region. Changes to four epidemiological parameters (latent period, duration of viraemia, probability of transmission from host to vector and virus replication) are sufficient to account for the rapid SBV spread within and between farms relative to that seen for BTV-8. This suggests that alternative transmission mechanisms (for example, direct transmission or additional vector species) are not necessary to explain the observed patterns of spread of SBV, though they may still play a minor role. The enhanced between-farm transmission of SBV brought about by these four parameters is such that the application of movement restrictions, even a total animal movement ban, would have little effect on the spread of SBV (relative reduction around 4 %).

The ability to estimate impact of Schmallenberg virus was restricted by the limited availability of data; studies conducted reported a probable effect of SBV infection on abortion, shorter gestation, non-return and the number of artificial inseminations required per animal. The principle economic impact of SBV has been felt via international trade restrictions, particularly in live animals and semen. Cattle semen trade has been restricted in several countries, in terms of percentage of total semen trade, most of the trades happens within the EU (2010: 73.4 % and 2011: 82.8 %). For the semen trade outside of the EU (2010: 26.6 % and 2011: 17.2 %), around 60 % of those are trade with countries imposing restrictions, representing for 2010 a 15.1 % of the total EU semen trade and for 2011 10.9 %. A decline between 11 and 26 % of the semen doses have been observed from previous years compared to 2012, as for the pure-bred breeding animals, the export value dropped 20 % in 2012 with respect to 2011 (http://www.adt.de/expla_fr.html).

Keywords

Schmallenberg virus (SBV), impact assessment, disease spread model