Schmallenberg Virus

Abstract

Schmallenberg virus (SBV) emerged in Northern Europe during summer 2011 and then caused a large epidemic in Europe. It is a negative‐sense single‐stranded RNA virus belonging to the Bunyaviridae family and the Orthobunyavirus genus. SBV affects predominantly domestic and wild ruminants and is transmitted by multiple species of Culicoides biting midges. SBV infection is mainly asymptomatic in adult cattle, sheep and goats but can cause congenital malformations, stillbirths and premature births when infection of the dam occurs at a critical period of gestation. In response to the emergence of SBV, molecular and serological tests have been generated rapidly to diagnose and monitor the disease and a number of inactivated vaccines have been developed.

Key Concepts

  • Schmallenberg virus (SBV) emerged in Northern Europe in summer 2011.
  • SBV belongs to the Bunyaviridae family and the Orthobunyavirus genus.
  • The SBV genome is composed of three negative‐sense single‐stranded RNA segments.
  • SBV is mainly asymptomatic in cattle, sheep and goats.
  • SBV is associated with abortion and birth of malformed or stillborn animals.
  • SBV is an arthropod‐borne virus transmitted by multiple species of Culicoides.
  • Several inactivated vaccines are available.

Keywords: Schmallenberg virus; Orthobunyavirus ; ruminants; emerging viral disease; congenital malformations; arbovirus

Figure 1. SBV morphology and genome organisation. (a) Schematic representation of a bunyavirus particle. The virion is enveloped and spherical with an approximate size of 80–120 nm in diameter. The genome is composed of three negative‐sense single‐stranded RNA segments: large (L), medium (M) and small (S). These segments form complexes with the nucleoprotein and the viral polymerase to constitute the viral RNPs. (b) Schematic representation of the SBV genome. Each viral segment is flanked by identical non‐coding sequences highly conserved between viral species belonging to the genus. These sequences are composed of complementary nucleotides able to pair up to form stable panhandle structures explaining the RNPs helical form in particle.
Figure 2. Orthobunyavirus replication strategy. For the genome replication step, all virion‐sense RNAs (vRNA) are used as templates by the L protein to produce complementary RNA (cRNA). cRNAs are replication intermediates that serve as template to produce neo‐formed vRNAs that will be packaged into new viral particles. mRNA transcription occurs via the same mechanism for all segments. The L protein begins mRNA transcription by a cap‐snatching mechanism, which consist in the cleavage of 5′capped nucleotides from cellular mature mRNAs to prime viral mRNA transcription. (a) L segment mRNA translation leads to the synthesis of the L protein without subsequent maturation steps. (b) M segment mRNA is translated as a polyprotein cleaved into three viral proteins: Gn, NSm and Gc. (c) S segment mRNA is translated in two proteins, N and NSs, by an overlapping reading frame.
Figure 3. SBV transmission cycle. (a) SBV is transmitted by biting midges belonging to the genus. These vectors become chronically infected with SBV after a blood meal on an infected animal. Infected vectors are able to spread infection to healthy livestock. (b) In case of adult animal infection, clinical manifestations are mild and associated with a short viraemia detectable from 2 to 6 days post‐infection. (c) When a pregnant female is infected, SBV has the ability to cross the placental barrier to infect several foetal tissues. In a few cases, foetal infection can lead to atypical foetal abnormalities, premature births or stillbirths.
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References

Balenghien T , Pagès N , Goffredo M , et al. (2014) The emergence of Schmallenberg virus across Culicoides communities and ecosystems in Europe. Preventive Veterinary Medicine 116 (4): 360–369.

Bangphoomi N , Takenaka‐Uema A , Sugi T , et al. (2014) Akabane virus utilizes alternative endocytic pathways to entry into mammalian cell lines. Journal of Veterinary Medical Science/the Japanese Society of Veterinary Science 76 (11): 1471–1478.

Barry G , Varela M , Ratinier M , et al. (2014) NSs protein of Schmallenberg virus counteracts the antiviral response of the cell by inhibiting its transcriptional machinery. Journal of General Virology 95: 1640–1646.

Bilk S , Schulze C , Fischer M , et al. (2012) Organ distribution of Schmallenberg virus RNA in malformed newborns. Veterinary Microbiology 159: 236–238.

Blomström A‐L , Stenberg H , Scharin I , et al. (2014) Serological screening suggests presence of Schmallenberg virus in cattle, sheep and goat in the Zambezia Province, Mozambique. Transboundary and Emerging Diseases 61: 289–292.

Bréard E , Lara E , Comtet L , et al. (2013) Validation of a commercially available indirect ELISA using a nucleocapside recombinant protein for detection of Schmallenberg virus antibodies. PLoS One 8: e53446.

Charles JA (1994) Akabane virus. The Veterinary Clinics of North America. Food Animal Practice 10: 525–546.

Claine F , Coupeau D , Wiggers L , Muylkens B and Kirschvink N (2013) Schmallenberg virus among female lambs, Belgium, 2012. Emerging Infectious Diseases 19: 1115–1117.

Coupeau D , Claine F , Wiggers L , et al. (2013a) Characterization of messenger RNA termini in Schmallenberg virus and related Simbuviruses. Journal of General Virology 94: 2399–2405.

Coupeau D , Claine F , Wiggers L , Kirschvink N and Muylkens B (2013b) In vivo and in vitro identification of a hypervariable region in Schmallenberg virus. Journal of General Virology 94: 1168–1174.

De Regge N , Deblauwe I , De Deken R , et al. (2012) Detection of Schmallenberg virus in different Culicoides spp. by real‐time RT‐PCR. Transboundary and Emerging Diseases 59: 471–475.

De Regge N , van den Berg T , Georges L and Cay B (2013) Diagnosis of Schmallenberg virus infection in malformed lambs and calves and first indications for virus clearance in the fetus. Veterinary Microbiology 162: 595–600.

Ducomble T , Wilking H , Stark K , et al. (2012) Lack of evidence for Schmallenberg virus infection in highly exposed persons, Germany, 2012. Emerging Infectious Diseases 18: 1333–1335.

EFSA (2014) Schmallenberg virus: state of art. EFSA Journal 12 (5): 3681.

Eifan S , Schnettler E , Dietrich I , Kohl A and Blomström A‐L (2013) Non‐structural proteins of arthropod‐borne bunyaviruses: roles and functions. Viruses 5: 2447–2468.

Elbers ARW , Meiswinkel R , van Weezep E , Sloet van Oldruitenborgh‐Oosterbaan MM and Kooi EA (2013) Schmallenberg virus in Culicoides spp. biting midges, the Netherlands, 2011. Emerging Infectious Diseases 19: 106–109.

Elbers ARW , Stockhofe‐Zurwieden N and van der Poel WHM (2014) Schmallenberg virus antibody persistence in adult cattle after natural infection and decay of maternal antibodies in calves. BMC Veterinary Research 10: 103.

Garigliany M‐M , Bayrou C , Kleijnen D , Cassart D and Desmecht D (2012) Schmallenberg virus in domestic cattle, Belgium, 2012. Emerging Infectious Diseases 18: 1512–1514.

Goller KV , Höper D , Schirrmeier H , Mettenleiter TC and Beer M (2012) Schmallenberg virus as possible ancestor of Shamonda virus. Emerging Infectious Diseases 18: 1644–1646.

Hahn K , Habierski A , Herder V , et al. (2013) Schmallenberg virus in central nervous system of ruminants. Emerging Infectious Diseases 19: 154–155.

Hechinger S , Wernike K and Beer M (2014) Single immunization with an inactivated vaccine protects sheep from Schmallenberg virus infection. Veterinary Research 45: 79.

Herder V , Wohlsein P , Peters M , Hansmann F and Baumgärtner W (2012) Salient lesions in domestic ruminants infected with the emerging so‐called Schmallenberg virus in Germany. Veterinary Pathology 49: 588–591.

Herder V , Hansmann F , Wohlsein P , et al. (2013) Immunophenotyping of inflammatory cells associated with Schmallenberg virus infection of the central nervous system of ruminants. PLoS One 8: e62939.

Hoffmann B , Scheuch M , Höper D , et al. (2012) Novel orthobunyavirus in Cattle, Europe, 2011. Emerging Infectious Diseases 18: 469–472.

Hoffmann B , Schulz C and Beer M (2013) First detection of Schmallenberg virus RNA in bovine semen, Germany, 2012. Veterinary Microbiology 167: 289–295.

Laloy E , Bréard E , Sailleau C , et al. (2014) Schmallenberg virus infection among red deer, France, 2010–2012. Emerging Infectious Diseases 20: 131–134.

Linden A , Desmecht D , Volpe R , et al. (2012) Epizootic spread of Schmallenberg virus among wild cervids, Belgium, Fall 2011. Emerging Infectious Diseases 18: 2006–2008.

Loeffen W , Quak S , de Boer‐Luijtze E , et al. (2012) Development of a virus neutralisation test to detect antibodies against Schmallenberg virus and serological results in suspect and infected herds. Acta Veterinaria Scandinavica 54: 44.

Mansfield KL , La Rocca SA , Khatri M , et al. (2013) Detection of Schmallenberg virus serum neutralising antibodies. Journal of Virological Methods 188: 139–144.

Ponsart C , Pozzi N , Bréard E , et al. (2014) Evidence of excretion of Schmallenberg virus in bull semen. Veterinary Research 45: 37.

Poskin A , Van Campe W , Mostin L , Cay B and De Regge N (2014) Experimental Schmallenberg virus infection of pigs. Veterinary Microbiology 170: 398–402.

Rasmussen LD , Kristensen B , Kirkeby C , et al. (2012) Culicoids as vectors of Schmallenberg virus. Emerging Infectious Diseases 18: 1204–1206.

Reusken C , van den Wijngaard C , van Beek P , et al. (2012) Lack of evidence for zoonotic transmission of Schmallenberg virus. Emerging Infectious Diseases 18: 1746–1754.

Saeed MF , Li L , Wang H , Weaver SC and Barrett AD (2001) Phylogeny of the Simbu serogroup of the genus Bunyavirus. Journal of General Virology 82: 2173–2181.

Sailleau C , Boogaerts C , Meyrueix A , et al. (2013a) Schmallenberg virus infection in dogs, France, 2012. Emerging Infectious Diseases 19: 1896–1898.

Sailleau C , Bréard E , Viarouge C , et al. (2013b) Acute Schmallenberg virus infections, France, 2012. Emerging Infectious Diseases 19: 321–322.

Schulz C , Wernike K , Beer M and Hoffmann B (2014) Infectious Schmallenberg virus from bovine semen, Germany. Emerging Infectious Diseases 20: 338–340.

Shi X , Kohl A , Léonard VHJ , et al. (2006) Requirement of the N‐terminal region of orthobunyavirus nonstructural protein NSm for virus assembly and morphogenesis. Journal of Virology 80: 8089–8099.

Taylor WP and Mellor PS (1994) The distribution of Akabane virus in the Middle East. Epidemiology and Infection 113: 175–185.

Van der Heijden HMJF , Bouwstra RJ , Mars MH , et al. (2013) Development and validation of an indirect Enzyme‐linked immunosorbent assay for the detection of antibodies against Schmallenberg virus in blood samples from ruminants. Research in Veterinary Science 95: 731–735.

Van Maanen C , van der Heijden H , Wellenberg GJ , et al. (2012) Schmallenberg virus antibodies in bovine and ovine fetuses. Veterinary Record 171: 299.

Varela M , Schnettler E , Caporale M , et al. (2013) Schmallenberg virus pathogenesis, tropism and interaction with the innate immune system of the host. PLoS Pathogens 9: e1003133.

Veldhuis AMB , Carp‐van Dijken S , van Wuijckhuise L , Witteveen G and van Schaik G (2014) Schmallenberg virus in Dutch dairy herds: potential risk factors for high within‐herd seroprevalence and malformations in calves, and its impact on productivity. Veterinary Microbiology 168: 281–293.

Veronesi E , Henstock M , Gubbins S , et al. (2013) Implicating Culicoides biting midges as vectors of Schmallenberg virus using semi‐quantitative RT‐PCR. PLoS One 8: e57747.

Wensman JJ , Blomqvist G , Hjort M and Holst BS (2013) Presence of antibodies to Schmallenberg virus in a dog in Sweden. Journal of Clinical Microbiology 51: 2802–2803.

Wernike K , Hoffmann B , Bréard E , et al. (2013a) Schmallenberg virus experimental infection of sheep. Veterinary Microbiology 166: 461–466.

Wernike K , Nikolin VM , Hechinger S , Hoffmann B and Beer M (2013b) Inactivated Schmallenberg virus prototype vaccines. Vaccine 31: 3558–3563.

Wernike K , Holsteg M , Schirrmeier H , Hoffmann B and Beer M (2014a) Natural infection of pregnant cows with Schmallenberg virus – a follow‐up study. PLoS One 9: e98223.

Yanase T , Maeda K , Kato T , et al. (2005) The resurgence of Shamonda virus, an African Simbu group virus of the genus Orthobunyavirus, in Japan. Archives of Virology 150: 361–369.

Yanase T , Kato T , Aizawa M , et al. (2012) Genetic reassortment between Sathuperi and Shamonda viruses of the genus Orthobunyavirus in nature: implications for their genetic relationship to Schmallenberg virus. Archives of Virology 157: 1611–1616.

Further Reading

Carpenter S , Groschup MH , Garros C , Felippe‐Bauer ML and Purse BV (2013) Culicoides biting midges, arboviruses and public health in Europe. Antiviral Research 100: 102–113.

Doceul V , Lara E , Sailleau C , et al. (2013) Epidemiology, molecular virology and diagnostics of Schmallenberg virus, an emerging orthobunyavirus in Europe. Veterinary Research 44: 31.

Walter CT and Barr JN (2011) Recent advances in the molecular and cellular biology of bunyaviruses. Journal of General Virology 92: 2467–2484.

Wernike K , Conraths F , Zanella G , et al. (2014) Schmallenberg virus—two years of experiences. Preventive Veterinary Medicine 116 (4): 423 – 434.

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How to Cite close
Doceul, Virginie, Gouzil, Julie, Vitour, Damien, and Zientara, Stéphan(Apr 2015) Schmallenberg Virus. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0024785]