1887

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Volume 98, Issue 7

Genetically stable infectious Schmallenberg virus persists in foetal envelopes of pregnant ewes Free

Abstract

Schmallenberg virus (SBV) is a recently emerged vector-borne virus, inducing congenital defects in bovines, ovines and caprines. Here we have shown that infectious SBV is capable of persisting until the moment of birth in the foetal envelopes of ewes infected with SBV-infectious serum at day 45 (1/5 positive) and 60 (4/6 positive) of gestation. This persistence of at least 100 days is a new aspect of the SBV pathogenesis that could help to explain how SBV overwinters the cold season in temperate climate zones. Furthermore, sequencing of the M segment shows that the persisting virus in the foetal envelopes is genetically stable since only a few mutations compared to the inoculum were found. This supports the hypothesis that persisting virus could start the infection of new hosts. Finally, neutralization tests showed that infectious SBV present in the foetal envelopes at birth can be neutralized by the humoral immunity present in the infected ewes.

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Keyword(s): overwintering , persistent infection , Schmallenberg virus , sequencing , sheep and virus isolation
© 2017 The Authors
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2017-07-01
2024-04-25
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References

  1. Hoffmann B, Scheuch M, Höper D, Jungblut R, Holsteg M et al. Novel orthobunyavirus in cattle, Europe, 2011. Emerg Infect Dis 2012; 18:469–472 [View Article][PubMed]
     [Google Scholar]
  2. Fischer M, Hoffmann B, Goller KV, Höper D, Wernike K et al. A mutation 'hot spot' in the schmallenberg virus M segment. J Gen Virol 2013; 94:1161–1167 [View Article][PubMed]
     [Google Scholar]
  3. Garigliany MM, Bayrou C, Kleijnen D, Cassart D, Jolly S et al. Schmallenberg virus: a new Shamonda/Sathuperi-like virus on the rise in Europe. Antiviral Res 2012; 95:82–87 [View Article][PubMed]
     [Google Scholar]
  4. Herder V, Wohlsein P, Peters M, Hansmann F, Baumgärtner W. Salient lesions in domestic ruminants infected with the emerging so-called Schmallenberg virus in Germany. Vet Pathol 2012; 49:588–591 [View Article][PubMed]
     [Google Scholar]
  5. van den Brom R, Luttikholt SJ, Lievaart-Peterson K, Peperkamp NH, Mars MH et al. Epizootic of ovine congenital malformations associated with Schmallenberg virus infection. Tijdschr Diergeneeskd 2012; 137:106–111[PubMed]
     [Google Scholar]
  6. Poskin A, Méroc E, Behaeghel I, Riocreux F, Couche M et al. Schmallenberg virus in Belgium: estimation of impact in cattle and sheep herds. Transbound Emerg Dis 2017; 64:264–274 [View Article][PubMed]
     [Google Scholar]
  7. de Regge N, de Deken R, Fassotte C, Losson B, Deblauwe I, Madder M et al. Culicoides monitoring in Belgium in 2011: analysis of spatiotemporal abundance, species diversity and Schmallenberg virus detection. Med Vet Entomol 2015; 29:263–275 [View Article][PubMed]
     [Google Scholar]
  8. Wernike K, Eschbaumer M, Breithaupt A, Hoffmann B, Beer M. Schmallenberg virus challenge models in cattle: infectious serum or culture-grown virus?. Vet Res 2012; 43:84 [View Article][PubMed]
     [Google Scholar]
  9. Wernike K, Eschbaumer M, Schirrmeier H, Blohm U, Breithaupt A et al. Oral exposure, reinfection and cellular immunity to Schmallenberg virus in cattle. Vet Microbiol 2013; 165:155–159 [View Article][PubMed]
     [Google Scholar]
  10. Wernike K, Hoffmann B, Bréard E, Bøtner A, Ponsart C et al. Schmallenberg virus experimental infection of sheep. Vet Microbiol 2013; 166:461–466 [View Article][PubMed]
     [Google Scholar]
  11. de Regge N, van den Berg T, Georges L, Cay B. Diagnosis of Schmallenberg virus infection in malformed lambs and calves and first indications for virus clearance in the fetus. Vet Microbiol 2013; 162:595–600 [View Article][PubMed]
     [Google Scholar]
  12. Martinelle L, Poskin A, dal Pozzo F, de Regge N, Cay B et al. Experimental infection of sheep at 45 and 60 days of gestation with Schmallenberg virus readily led to placental colonization without causing congenital malformations. PLoS One 2015; 10:e0139375 [View Article][PubMed]
     [Google Scholar]
  13. Cay AB, de Regge N, Riocreux F, Meroc E, van der Stede Y et al. Le virus Schmallenberg en Belgique: premiers diagnostics et premières évaluations. Nouveau Practicien Vétérinaire 2012; 5:29–34
     [Google Scholar]
  14. Hulst M, Kortekaas J, Hakze-van der Honing R, Vastenhouw S, Cornellissen J et al. Genetic characterization of an atypical Schmallenberg virus isolated from the brain of a malformed lamb. Virus Genes 2013; 47:505–514 [View Article][PubMed]
     [Google Scholar]
  15. Mehta S, Rajput YS. Immunosuppressive activity in buffalo placenta. Indian J Exp Biol 1999; 37:959–964[PubMed]
     [Google Scholar]
  16. Bilk S, Schulze C, Fischer M, Beer M, Hlinak A et al. Organ distribution of Schmallenberg virus RNA in malformed newborns. Vet Microbiol 2012; 159:236–238 [View Article][PubMed]
     [Google Scholar]
  17. Coupeau D, Claine F, Wiggers L, Kirschvink N, Muylkens B. In vivo and in vitro identification of a hypervariable region in Schmallenberg virus. J Gen Virol 2013; 94:1168–1174 [View Article][PubMed]
     [Google Scholar]
  18. Coupeau D, Claine F, Wiggers L, Kirschvink N, Muylkens B. S segment variability during the two first years of the spread of Schmallenberg virus. Arch Virol 2016; 161:1353–1358 [View Article][PubMed]
     [Google Scholar]
  19. Hofmann MA, Mader M, Flückiger F, Renzullo S. Genetic stability of Schmallenberg virus in vivo during an epidemic, and in vitro, when passaged in the highly susceptible porcine SK-6 cell line. Vet Microbiol 2015; 176:97–108 [View Article][PubMed]
     [Google Scholar]
  20. Wernike K, Hoffmann B, Conraths FJ, Beer M. Schmallenberg virus recurrence Germany, 2014. Emerg Infect Dis 2015; 21:1202–1204 [View Article][PubMed]
     [Google Scholar]
  21. Izzo F, Cosseddu GM, Polci A, Iapaolo F, Pinoni C et al. Genetic characterization of Italian field strains of Schmallenberg virus based on N and NSs genes. Virus Genes 2016; 52:582–585 [View Article][PubMed]
     [Google Scholar]
  22. Doceul V, Lara E, Sailleau C, Belbis G, Richardson J et al. Epidemiology, molecular virology and diagnostics of Schmallenberg virus, an emerging orthobunyavirus in Europe. Vet Res 2013; 44:31 [View Article][PubMed]
     [Google Scholar]
  23. Ebel GD, Carricaburu J, Young D, Bernard KA, Kramer LD. Genetic and phenotypic variation of West Nile virus in New York, 2000–2003. Am J Trop Med Hyg 2004; 71:493–500[PubMed]
     [Google Scholar]
  24. Davis CT, Ebel GD, Lanciotti RS, Brault AC, Guzman H et al. Phylogenetic analysis of North American West Nile virus isolates, 2001–2004: evidence for the emergence of a dominant genotype. Virology 2005; 342:252–265 [View Article][PubMed]
     [Google Scholar]
  25. Parameswaran P, Charlebois P, Tellez Y, Nunez A, Ryan EM et al. Genome-wide patterns of intrahuman dengue virus diversity reveal associations with viral phylogenetic clade and interhost diversity. J Virol 2012; 86:8546–8558 [View Article][PubMed]
     [Google Scholar]
  26. Forrester NL, Coffey LL, Weaver SC. Arboviral bottlenecks and challenges to maintaining diversity and fitness during mosquito transmission. Viruses 2014; 6:3991–4004 [View Article][PubMed]
     [Google Scholar]
  27. Eisen HN. Affinity enhancement of antibodies: how low-affinity antibodies produced early in immune responses are followed by high-affinity antibodies later and in memory B-cell responses. Cancer Immunol Res 2014; 2:381–392 [View Article][PubMed]
     [Google Scholar]
  28. Zimmer JY, Haubruge E, Francis F, Bortels J, Simonon G et al. Breeding sites of bluetongue vectors in northern Europe. Vet Rec 2008; 162:131 [View Article][PubMed]
     [Google Scholar]
  29. Zimmer JY, Saegerman C, Losson B, Haubruge E. Breeding sites of bluetongue virus vectors, Belgium. Emerg Infect Dis 2010; 16:575–576 [View Article][PubMed]
     [Google Scholar]
  30. Koenraadt CJ, Balenghien T, Carpenter S, Ducheyne E, Elbers AR et al. Bluetongue, Schmallenberg – what is next? Culicoides-borne viral diseases in the 21st Century. BMC Vet Res 2014; 10:77 [View Article][PubMed]
     [Google Scholar]
  31. Martinelle L, Poskin A, dal Pozzo F, Mostin L, van Campe W et al. Three different routes of inoculation for experimental infection with Schmallenberg virus in sheep. Transbound Emerg Dis 2017; 64:305–308 [View Article][PubMed]
     [Google Scholar]
  32. Alexander KA, Maclachlan NJ, Kat PW, House C, O'Brien SJ et al. Evidence of natural bluetongue virus infection among African carnivores. Am J Trop Med Hyg 1994; 51:568–576 [View Article][PubMed]
     [Google Scholar]
  33. Jauniaux TP, de Clercq KE, Cassart DE, Kennedy S, Vandenbussche FE et al. Bluetongue in Eurasian lynx. Emerg Infect Dis 2008; 14:1496–1498 [View Article][PubMed]
     [Google Scholar]
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Genetically stable infectious Schmallenberg virus persists in foetal envelopes of pregnant ewes
J. Gen. Virol. 98, 1630 (2017); https://doi.org/10.1099/jgv.0.000841
/content/journal/jgv/10.1099/jgv.0.000841
/content/journal/jgv/10.1099/jgv.0.000841
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