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 Sep 29;10(9):e0139375. doi: 10.1371/journal.pone.0139375. eCollection 2015.

Abstract

Background: Main impact of Schmallenberg virus (SBV) on livestock consists in reproductive disorders, with teratogenic effects, abortions and stillbirths. SBV pathogenesis and viral placental crossing remain currently poorly understood. Therefore, we implemented an experimental infection of ewes, inoculated with SBV at 45 or 60 days of gestation (dg).

Methodology: "Mourerous" breed ewes were randomly separated in three groups: eight and nine ewes were subcutaneously inoculated with 1 ml of SBV infectious serum at 45 and 60 dg, respectively (G45 and G60). Six other ewes were inoculated subcutaneously with sterile phosphate buffer saline as control group. All SBV inoculated ewes showed RNAemia consistent with previously published studies, they seroconverted and no clinical sign was reported. Lambs were born at term via caesarian-section, and right after birth they were blood sampled and clinically examined. Then both lambs and ewes were euthanatized and necropsied.

Principal findings/significance: No lambs showed any malformation suggestive of SBV infection and none of them had RNAemia or anti-SBV antibodies prior to colostrum uptake. Positive SBV RNA detection in organs was rare in both G45 and G60 lambs (2/11 and 1/10, respectively). Nevertheless most of the lambs in G45 (9/11) and G60 (9/10) had at least one extraembryonic structure SBV positive by RTqPCR. The number of positive extraembryonic structures was significantly higher in G60 lambs. Time of inoculation (45 or 60 dg) had no impact on the placental colonization success rate but affected the frequency of detecting the virus in the offspring extraembryonic structures by the time of lambing. SBV readily colonized the placenta when ewes were infected at 45 or 60 dg but infection of the fetuses was limited and did not lead to congenital malformations.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Antibodies, Viral / blood
  • Antibodies, Viral / immunology
  • Bunyaviridae Infections / blood
  • Bunyaviridae Infections / veterinary
  • Bunyaviridae Infections / virology*
  • Chlorocebus aethiops
  • Congenital Abnormalities / veterinary
  • Congenital Abnormalities / virology*
  • Female
  • Gestational Age
  • Infectious Disease Transmission, Vertical / veterinary
  • Male
  • Orthobunyavirus / genetics
  • Orthobunyavirus / immunology
  • Orthobunyavirus / physiology*
  • Placenta / virology*
  • Pregnancy
  • RNA, Viral / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sheep
  • Sheep Diseases / diagnosis
  • Sheep Diseases / transmission
  • Sheep Diseases / virology*
  • Time Factors
  • Vero Cells

Substances

  • Antibodies, Viral
  • RNA, Viral

Grants and funding

This study was financially supported by Federal Public Service Public Health and Safety of the Food Chain and Environment (RF12/6270), and the European Union as outlined in Council Decision 2012/349/EU concerning a financial contribution by the Union for studies on Schmallenberg virus. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.