Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Viral emergence and consequences for reproductive performance in ruminants: two recent examples (bluetongue and Schmallenberg viruses)

Stéphan Zientara A C and Claire Ponsart B
+ Author Affiliations
- Author Affiliations

A UPE, ANSES, INRA, ENVA, UMR 1161 ANSES/INRA/ENVA, Laboratoire de santé animale d’Alfort, 23 Avenue du Général de gaulle, 94703 Maisons-Alfort, France.

B ANSES, Unité des zoonoses bactériennes, Laboratoire de santé animale d’Alfort, 23 Avenue du Général de gaulle, 94703 Maisons-Alfort, France.

C Corresponding author. Email: s.zientara@afssa.fr

Reproduction, Fertility and Development 27(1) 63-71 https://doi.org/10.1071/RD14367
Published: 4 December 2014

Abstract

Viruses can emerge unexpectedly in different regions of the world and may have negative effects on reproductive performance. This paper describes the consequences for reproductive performance that have been reported after the introduction to Europe of two emerging viruses, namely the bluetongue (BTV) and Schmallenberg (SBV) viruses. Following the extensive spread of BTV in northern Europe, large numbers of pregnant cows were infected with BTV serotype 8 (BTV-8) during the breeding season of 2007. Initial reports of some cases of abortion and hydranencephaly in cattle in late 2007 were followed by quite exhaustive investigations in the field that showed that 10%–35% of healthy calves were infected with BTV-8 before birth. Transplacental transmission and fetal abnormalities in cattle and sheep had been previously observed only with strains of the virus that were propagated in embryonated eggs and/or cell culture, such as vaccine strains or vaccine candidate strains. After the unexpected emergence of BTV-8 in northern Europe in 2006, another arbovirus, namely SBV, emerged in Europe in 2011, causing a new economically important disease in ruminants. This new virus, belonging to the Orthobunyavirus genus in the Bunyaviridae family, was first detected in Germany, in The Netherlands and in Belgium in 2011 and soon after in the UK, France, Italy, Luxembourg, Spain, Denmark and Switzerland. Adult animals show no or only mild clinical symptoms, whereas infection during a critical period of gestation can lead to abortion, stillbirth or the birth of severely malformed offspring. The impact of the disease is usually greater in sheep than in cattle. The consequences of SBV infection in domestic ruminants and more precisely the secondary effects on off-springs will be described.

Additional keywords: abortion, infertility.


References

Acree, J. A., Echternkamp, S. E., Kappes, S. M., Luedke, A. J., Holbrook, F. R., Pearson, J. E., and Ross, G. S. (1991). Failure of embryos from bluetongue infected cattle to transmit virus to susceptible recipients of their offspring. Theriogenology 36, 689–697.
Failure of embryos from bluetongue infected cattle to transmit virus to susceptible recipients of their offspring.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFyjsw%3D%3D&md5=691d6081342d44b6ad811785f9429f05CAS | 16727038PubMed |

Ali Al Ahmad, M. Z., Pellerin, J. L., Larrat, M., Chatagnon, G., Cécile, R., and Sailleau, C. (2011). Can bluetongue virus (BTV) be transmitted via caprine embryo transfer? Theriogenology 76, 126–132.
Can bluetongue virus (BTV) be transmitted via caprine embryo transfer?Crossref | GoogleScholarGoogle Scholar |

Ali Al Ahmad, M. Z., Bruyas, J. F., Pellerin, J. L., Larrat, M., Chatagnon, G., Roux, C., Sailleau, C., Zientara, S., and Fieni, F. (2012). Evaluation of bluetongue virus (BTV) decontamination techniques for caprine embryos produced in vivo. Theriogenology 78, 1286–1293.
Evaluation of bluetongue virus (BTV) decontamination techniques for caprine embryos produced in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtF2ru73P&md5=c8acf5987730b8fbc29067d632f56f70CAS |

Backx, A., Heutink, R., van Rooij, E., and van Rijn, P. (2009). Transplacental and oral transmission of wild-type bluetongue virus serotype 8 in cattle after experimental infection. Vet. Microbiol. 138, 235–243.
Transplacental and oral transmission of wild-type bluetongue virus serotype 8 in cattle after experimental infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2ksLvN&md5=86d27756b523972a632aa261baa48299CAS | 19419822PubMed |

Barratt-Boyes, S. M., and MacLachlan, N. J. (1994). Dynamics of viral spread in bluetongue virus infected calves Vet. Microbiol. 40, 361–371.
Dynamics of viral spread in bluetongue virus infected calvesCrossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2FislKlsg%3D%3D&md5=3765dfd892a2c420292ff3038931131bCAS | 7941299PubMed |

Bilk, S., Schulze, C., Fischer, M., Beer, M., Hlinak, A., and Hoffmann, B. (2012). Organ distribution of Schmallenberg virus RNA in malformed newborns. Vet. Microbiol. 159, 236–238.
Organ distribution of Schmallenberg virus RNA in malformed newborns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvVSms78%3D&md5=dac2bce6844ac55780a72295edd96735CAS | 22516190PubMed |

Bonneau, K. R., and MacLachlan, N. J. (2004). Genetic diversification of field strains for bluetongue virus. Vet. Ital. 40, 446–447.
| 1:STN:280:DC%2BC3c3ptFCgsw%3D%3D&md5=02d671bbda210d042e1593c4a9255159CAS | 20422567PubMed |

Bonneau, K. R., Zhang, N., Zhu, J., Zhang, F., Li, Z., Zhang, K., Xiao, L., Xing, W., and MacLachlan, N. J. (1999). Sequence comparison of the L2 and S10 genes of bluetongue viruses from the United States and the People’s Republic of China. Virus Res. 61, 153–160.
Sequence comparison of the L2 and S10 genes of bluetongue viruses from the United States and the People’s Republic of China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Ort7s%3D&md5=0b04756da3e865429abd1d8aa3fd4898CAS | 10475085PubMed |

Bonneau, K. R., Mullens, B. A., and MacLachlan, N. J. (2001). Occurrence of genetic drift and founder effect during quasispecies evolution of the VP2 and NS3/3A genes of bluetongue virus upon passage between sheep and cattle. J. Virol. 75, 8298–8305.
Occurrence of genetic drift and founder effect during quasispecies evolution of the VP2 and NS3/3A genes of bluetongue virus upon passage between sheep and cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtFeju7s%3D&md5=195fa043386335bc20626d2fb67ad517CAS | 11483775PubMed |

Bouwstra, R. J., Kooi, E. A., de Kluijver, E. P., Verstraten, E. R., Bongers, J. H., van Maanen, C., Wellenberg, G. J., van der Spek, A. N., and van der Poel, W. H. (2013). Schmallenberg virus outbreak in The Netherlands: routine diagnostics and test results. Vet. Microbiol. 165, 102–108.
Schmallenberg virus outbreak in The Netherlands: routine diagnostics and test results.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3svpsFentg%3D%3D&md5=b4c8ca8cb0d28f41d4c8fbbd7445a597CAS | 23528650PubMed |

Bréard, E., Hamblin, C., Hammoumi, S., Sailleau, C., Dauphin, G., and Zientara, S. (2004). The epidemiology and diagnosis of bluetongue with particular reference to Corsica. Res. Vet. Sci. 77, 1–8.
The epidemiology and diagnosis of bluetongue with particular reference to Corsica.Crossref | GoogleScholarGoogle Scholar | 15120946PubMed |

Calistri, P., Giovannini, A., Conte, A., Nannini, D., Santucci, U., Patta, C., Rolesu, S., and Caporale, V. (2004). Bluetongue in Italy: part I. Vet. Ital. 40, 243–251.
| 1:STN:280:DC%2BC3c3ovVemtw%3D%3D&md5=1189df069756f8498838eca22ba4d36bCAS | 20419672PubMed |

De Clercq, K., De Leeuw, I., Verheyden, B., Vandemeulebroucke, E., Vanbinst, T., Herr, C., Meroc, E., Bertels, G., Steurbaut, N., Miry, C., De Bleecker, K., Maquet, G., Bughin, J., Saulmont, M., Lebrun, M., Sustronck, B., De Deken, R., Hooyberghs, J., Houdart, P., Raemaekers, M., Mintiens, K., Kerkhofs, P., Goris, N., and Vandenbussche, F. (2008). Transplacental infection and apparently immunotolerance induced by a wild-type bluetongue virus serotype 8 natural infection. Transbound Emerg. Dis. 55, 352–359.
Transplacental infection and apparently immunotolerance induced by a wild-type bluetongue virus serotype 8 natural infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1crpslyqtg%3D%3D&md5=e0e05078ea04de6ddbaa32496f6d688bCAS | 18673339PubMed |

DeMaula, C. D., Leutenegger, C. M., Bonneau, K. R., and MacLachlan, N. J. (2002). The role of endothelial cell-derived inflammatory and vasoactive mediators in the pathogenesis of bluetongue. Virology 296, 330–337.
The role of endothelial cell-derived inflammatory and vasoactive mediators in the pathogenesis of bluetongue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksFOgtbc%3D&md5=8e62d3ca8647cfc8f61ed7c7c28e843cCAS | 12069531PubMed |

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. Vet. Microbiol. 162, 595–600.
Diagnosis of Schmallenberg virus infection in malformed lambs and calves and first indications for virus clearance in the fetus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvFWhu7jN&md5=49c76e1361056efc5297bfc3753e2871CAS | 23265245PubMed |

Desmecht, D., Bergh, R. V., Sartelet, A., Leclerc, M., Mignot, C., Misse, F., Sudraud, C., Berthemin, S., Jolly, S., Mousset, B., Linden, A., Coignoul, F., and Cassart, D. (2008). Evidence for transplacental transmission of the current wild-type strain of bluetongue virus serotype 8 in cattle. Vet. Rec. 163, 50–52.
Evidence for transplacental transmission of the current wild-type strain of bluetongue virus serotype 8 in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvkvVensg%3D%3D&md5=97c4d14342da1522eb2eb0e22c7a730fCAS | 18621997PubMed |

Doceul, V., Lara, E., Sailleau, C., Belbis, G., Richardson, J., Breard, E., Viarouge, C., Dominguez, M., Hendrikx, P., Calavas, D., Desprat, A., Languille, J., Comtet, L., Pourquier, P., Eleouët, J. F., Delmas, B., Marianneau, P., Vitour, D., and Zientara, S. (2013). Epidemiology, molecular virology and diagnostics of Schmallenberg virus. Vet. Res. 44, 31.
Epidemiology, molecular virology and diagnostics of Schmallenberg virus.Crossref | GoogleScholarGoogle Scholar | 23675914PubMed |

Elbers, A. R., Loeffen, W. L., Quak, S., de Boer-Luijtze, E., van der Spek, A. N., Bouwstra, R., Maas, R., Spierenburg, M. A., de Kluijver, E. P., van Schaik, G., and van der Poel, W. H. (2012). Seroprevalence of Schmallenberg virusantibodies among dairy cattle, the Netherlands, winter 2011–2012. Emerg. Infect. Dis. 18, 1065–1071.
| 22709656PubMed |

European Food Safety Authority (2011). Scientific opinion on bluetongue serotype 8. EFSA J. 9, 2189.

Foster, N. M., Alders, M. A., Luedke, A. J., and Walton, T. E. (1980). Abnormalities and virus-like particles in spermatozoa from bulls latently infected with bluetongue virus. Am. J. Vet. Res. 41, 1045–1048.
| 1:STN:280:DyaL3M%2FmtVGisw%3D%3D&md5=07650a509022bbca9bf3c9a538ba1cbeCAS | 6254406PubMed |

Garigliany, M. M., Hoffmann, B., Dive, M., Sartelet, A., Bayrou, C., Cassart, D., Beer, M., and Desmecht, D. (2012). Schmallenberg virus in calf born at term with porencephaly, belgium. Emerg. Infect. Dis. 18, 1005–1006.
| 22607989PubMed |

Gibbens, N. (2012). Schmallenberg virus: a novel viral disease in northern Europe. Vet. Rec. 170, 58.
Schmallenberg virus: a novel viral disease in northern Europe.Crossref | GoogleScholarGoogle Scholar | 22247205PubMed |

Gibbs, E. P. J., and Greiner, E. C. (1994). The epidemiology of bluetongue. Comp. Immunol. Microbiol. Infect. Dis. 17, 207–220.
The epidemiology of bluetongue.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2FpsVCqtA%3D%3D&md5=6c1325c9fd1a3215ff848c7d6a741886CAS |

Gilbert, R. O., Coubrough, R. I., and Weiss, K. E. (1987). The transmission of bluetongue virus by embryo transfer in sheep. Theriogenology 27, 527–540.
The transmission of bluetongue virus by embryo transfer in sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFShsQ%3D%3D&md5=94c34c3113e5180d61ad61e260dece3bCAS | 16726257PubMed |

Hahn, K., Habierski, A., Herder, V., Wohlsein, P., Peters, M., Hansmann, F., and Baumgartner, W. (2013). Schmallenberg virus in central nervous system of ruminants. Emerg. Infect. Dis. 19, 154–155.
Schmallenberg virus in central nervous system of ruminants.Crossref | GoogleScholarGoogle Scholar | 23260872PubMed |

Hare, W. C. D., Luedke, A. J., Thomas, F. C., Bowen, R. A., Singh, E. L., Eaglesome, M. D., Randall, G. C. B., and Bielanski, A. (1988). Nontransmission of bluetongue virus by embryos from bluetongue virus-infected sheep. Am. J. Vet. Res. 49, 468–472.
| 1:STN:280:DyaL1c3jvFWqsw%3D%3D&md5=930d68efd2ec25304c8d3eecc2a13745CAS |

Hoffmann, B., Scheuch, M., Hoper, D., Jungblut, R., Holsteg, M., Schirrmeier, H., Eschbaumer, M., Goller, K. V., Wernike, K., Fischer, M., Breithaupt, A., Mettenleiter, T. C., and Beer, M. (2012). Novel orthobunyavirus in cattle, Europe, 2011. Emerg. Infect. Dis. 18, 469–472.
Novel orthobunyavirus in cattle, Europe, 2011.Crossref | GoogleScholarGoogle Scholar | 22376991PubMed |

Hoffmann, B., Schulz, C., and Beer, M. (2013). First detection of Schmallenberg virus RNA in bovine semen, Germany, 2012. Vet. Microbiol. 167, 289–295.
First detection of Schmallenberg virus RNA in bovine semen, Germany, 2012.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFOgu7zP&md5=b8d8a61f526a4d64a7ad31f3fcbdff14CAS | 24100006PubMed |

Howard, T. H., Bowen, R. A., and Pickett, B. W. (1985). Isolation of bluetongue virus from bull semen. Prog. Clin. Biol. Res. 178, 127–134.
| 1:STN:280:DyaL2M3kt1Oqsg%3D%3D&md5=1edb71eff1bd7a98baa63202c05b4471CAS | 2989846PubMed |

Kirkbride, C. A., and Johnson, M. W. (1989). Serologic examination of aborted ovine and bovine fetal fluids for the diagnosis of border disease, bluetongue, bovine viral diarrhea, and leptospiral infections. J. Vet. Diagn. Invest. 1, 132–138.
| 1:STN:280:DyaK3M7nsF2ntQ%3D%3D&md5=7a046452c4b4d4f7197b2d240d0689e0CAS | 2562192PubMed |

Kirkland, P. D., Barry, R. D., Harper, P. A., and Zelski, R. Z. (1988). The development of Akabane virus-induced congenital abnormalities in cattle. Vet. Rec. 122, 582–586.
The development of Akabane virus-induced congenital abnormalities in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1czit1OltQ%3D%3D&md5=333aa71744c34c15a607028df6040e3dCAS | 3137718PubMed |

Kirschvink, N., Raes, M., and Saegerman, C. (2008). Impact of a natural bluetongue serotype 8 infection on semen quality of rams (Belgium, 2007). Renc. Rech. Ruminants 15, 35.

Le Gal, M. C., Dufour, B., Geoffroy, E., Zanella, G., Moutou, F., Millemann, Y., Rieffel, J. N., and Pouilly, F. (2008). Bluetongue virus serotype 8 in the Ardennes in 2007. Vet. Rec. 163, 668.
Bluetongue virus serotype 8 in the Ardennes in 2007.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnsVCqsQ%3D%3D&md5=8e246ffdffa15f985a4a728534c9a1d4CAS | 19043098PubMed |

Loeffen, W., Quak, S., de Boer-Luijtze, E., Hulst, M., van der Poel, W., Bouwstra, R., and Maas, R. (2012). Development of a virus neutralisation test to detect antibodies against Schmallenberg virus and serological results in suspect and infected herds. Acta Vet. Scand. 54, 44.
Development of a virus neutralisation test to detect antibodies against Schmallenberg virus and serological results in suspect and infected herds.Crossref | GoogleScholarGoogle Scholar | 22871162PubMed |

MacLachlan, N. J., and Guthrie, A. J. (2010). Re-emergence of bluetongue, African horse sickness, and other Orbivirus diseases. Vet. Res. 41, 35.
Re-emergence of bluetongue, African horse sickness, and other Orbivirus diseases.Crossref | GoogleScholarGoogle Scholar | 20167199PubMed |

MacLachlan, N. J., Conley, A. J., and Kennedy, P. C. (2000). Bluetongue and equine viral arteritis viruses as models of virus-induced fetal injury and abortion. Anim. Reprod. Sci. 60–61, 643–651.
Bluetongue and equine viral arteritis viruses as models of virus-induced fetal injury and abortion.Crossref | GoogleScholarGoogle Scholar | 10844231PubMed |

MacLachlan, N. J., Drew, C. P., Darpel, K. E., and Worwa, G. (2009). The pathology and pathogenesis of bluetongue. J. Comp. Pathol. 141, 1–16.
| 1:CAS:528:DC%2BD1MXmvFajurc%3D&md5=fb7bcf67960bce96d4ed06a50a88aec0CAS | 19476953PubMed |

Mertens, P. P., Diprose, J., Maan, S., Singh, K. P., Attoui, H., and Samuel, A. R. (2004). Bluetongue virus replication, molecular and structural biology. Vet. Ital. 40, 426–437.
| 1:STN:280:DC%2BC3c3ptFChuw%3D%3D&md5=4c66480ae66884ee95140bdb087b9904CAS | 20422565PubMed |

Müller, U., Kemmerling, K., Straet, D., Janowitz, U., and Sauerwein, H. (2010). Effects of bluetongue virus infection on sperm quality in bulls: a preliminary report. Vet. J. 186, 402–403.
Effects of bluetongue virus infection on sperm quality in bulls: a preliminary report.Crossref | GoogleScholarGoogle Scholar | 19850499PubMed |

Ponsart, C., Pozzi, N., Bréard, E., Catinot, V., Viard, G., Sailleau, C., Viarouge, C., Gouzil, J., Beer, M., Zientara, S., and Vitour, D. (2014). Evidence of excretion of Schmallenberg virus in bull semen. Vet. Res. 45, 37.
Evidence of excretion of Schmallenberg virus in bull semen.Crossref | GoogleScholarGoogle Scholar | 24708245PubMed |

Pritchard, L. I., Sendow, I., Lunt, R., Hassan, S. H., Kattenbelt, J., Gould, A. R., Daniels, P. W., and Eaton, B. T. (2004). Genetic diversity of bluetongue viruses in south east Asia. Virus Res. 101, 193–201.
Genetic diversity of bluetongue viruses in south east Asia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisVKlsL8%3D&md5=79daf3b6c98fc2ab8d1474404435a6a3CAS | 15041187PubMed |

ProMed-mail. (2012a). ‘Schmallenberg virus–Europe (76) virus RNA in bovine semen.’ Available at: http://promedmail.org/direct.php?id=20121220.1460864 [verified 20 December 2012].

ProMed-mail. (2012b). ‘Schmallenberg virus–Europe (77) (NL, FR) virus RNA in bovine semen.’ Available at: http://promedmail.org/direct.php?id=20121221.1462748 [verified 20 December 2012].

Rasmussen, L. D., Savini, G., Lorusso, A., Bellacicco, A., Palmarini, M., Caporale, M., Rasmussen, T. B., Belsham, G. J., and Bøtner, A. (2013). Transplacental transmission of field and rescued strains of BTV-2 and BTV-8 in experimentally infected sheep. Vet Res. 44, 75.
Transplacental transmission of field and rescued strains of BTV-2 and BTV-8 in experimentally infected sheep.Crossref | GoogleScholarGoogle Scholar | 24007601PubMed |

Roeder, P. L., Taylor, W. P., Roberts, D. H., Wood, L., Jeggo, M. H., Gard, G. P., Corteyn, M., and Graham, S. (1991). Failure to establish congenital bluetongue virus infection by infecting cows in early pregnancy. Vet. Rec. 128, 301–304.
Failure to establish congenital bluetongue virus infection by infecting cows in early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3ktVKjtA%3D%3D&md5=4d1d085919683159f930b005349757b6CAS | 1852081PubMed |

Saeed, M. F., Li, L., Wang, H., Weaver, S. C., and Barrett, A. D. (2001). Phylogenyof the Simbu serogroup of the genus Bunyavirus. J. Gen. Virol. 82, 2173–2181.
| 1:CAS:528:DC%2BD3MXmslSktb8%3D&md5=5380c58ef2a3d2daf6b77a2c4c78a9daCAS | 11514727PubMed |

Saegerman, C., Martinelle, L., Dal Pozzo, F., and Kirschvink, N. (2013). Preliminary survey on the impact of Schmallenberg virus on sheep flocks in south of Belgium. Transbound. Emerg. Dis. 61, 469–472.
Preliminary survey on the impact of Schmallenberg virus on sheep flocks in south of Belgium.Crossref | GoogleScholarGoogle Scholar | 23294537PubMed |

Sailleau, C., Breard, E., Viarouge, C., Desprat, A., Doceul, V., Lara, E., Languille, J., Vitour, D., Attoui, H., and Zientara, S. (2013). Acute Schmallenberg virus infections, France, 2012. Emerg. Infect. Dis. 19, 321–322.
Acute Schmallenberg virus infections, France, 2012.Crossref | GoogleScholarGoogle Scholar | 23460989PubMed |

Savini, G., Maclachlan, N. J., Calistri, P., Sanchez-Vizcaino, J. M., and Zientara, S. (2008). Vaccines against bluetongue in Europe. Comp. Immunol. Microbiol. Infect. Dis. 31, 101–120.
| 17765305PubMed |

Schlafer, D. H., Gillespie, J. H., Foote, R. H., Quick, S., Pennow, N. N., Dougherty, E. P., Schiff, E. I., Allen, S. E., Powers, P. A., Hall, C. E., and Voss, H. (1990). Experimental transmission of bovine viral diseases by insemination with contaminated semen or during embryo transfer. Dtsch. Tierarztl. Wochenschr. 97, 68–72.
| 1:STN:280:DyaK3c7otlOksA%3D%3D&md5=a8130f4a478bf59d83cacbfaad51f2d1CAS | 2155769PubMed |

Schwartz-Cornil, I., Mertens, P. P. C., Contreras, V., Hemati, B., Pascale, F., Bréard, E., Mellor, P., Maclachlan, N. J., and Zientara, S. (2008). Bluetongue virus: virology, physiopathology and immunity. Vet. Res. 39, 46.
Bluetongue virus: virology, physiopathology and immunity.Crossref | GoogleScholarGoogle Scholar | 18495078PubMed |

Singh, E. L., Eaglesome, M. D., Thomas, F. C., Papp-Vid, G., and Hare, W. C. (1982). Embryo transfer as a means of controlling the transmission of viral infections. I. The in vitro exposure of preimplantation bovine embryos to akabane, bluetongue and bovine viral diarrhea viruses. Theriogenology 17, 437–444.
Embryo transfer as a means of controlling the transmission of viral infections. I. The in vitro exposure of preimplantation bovine embryos to akabane, bluetongue and bovine viral diarrhea viruses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVCrsw%3D%3D&md5=b4865e7b70f70b65c05147c5a7241ee3CAS | 16725707PubMed |

Singh, E. L., Dulac, G. C., and Henderson, J. M. (1997). Embryo transfer as a means of controlling the transmission of viral infections. XV. Failure to transmit bluetongue virus through the transfer embryos from viremic sheep donors. Theriogenology 47, 1205–1214.
Embryo transfer as a means of controlling the transmission of viral infections. XV. Failure to transmit bluetongue virus through the transfer embryos from viremic sheep donors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVyhsw%3D%3D&md5=ef7a949dc7d2fd2c79fc31bed6d34110CAS | 16728069PubMed |

Steinrigl, A., Hoffmann, B., Wodak, E., and Schmoll, F. (2013). Detection of Schmallenberg virus genome in semen of Austrian bulls. In ‘Proceedings of the 7th Annual Meeting of EPIZONE, 1–4 October 2013, Brussels’. (Eds CODA-CERVA.) p. 173 [Abstract]. (CODA-CERVA: Brussels.)

Stockhofe, N., Hulst, M., Hakze, R., Vellema, P., and van der Poel W. (2013). Transplacental infection of Schmallenberg virus in the first trimester of gestation is highly efficient in sheep. In ‘Proceedings of the 7th Annual Meeting of EPIZONE, 1–4 October 2013, Brussels’. p. 77 [Abstract]. (Veterinaria Italiana: City of Teramo, Italy.)

Tabachnick, W. J. (2004). Culicoides and the global epidemiology of bluetongue virus infection. Vet. Ital. 40, 144–150.
| 1:STN:280:DC%2BC3c3ovVegtA%3D%3D&md5=329c1d1994e4eb853c0ccb7b4475b891CAS | 20419653PubMed |

Thomas, F. C., Singh, E. L., and Hare, W. C. D. (1983). Embryo transfer as a means of controlling viral infections. III. Non transmission of bluetongue virus from viremic cattle. Theriogenology 19, 425–431.
Embryo transfer as a means of controlling viral infections. III. Non transmission of bluetongue virus from viremic cattle.Crossref | GoogleScholarGoogle Scholar |

Thomas, F. C., Singh, E. L., and Hare, W. C. (1985). Embryo transfer as a means of controlling viral infections. VI. Bluetongue virus-free calves from infectious semen. Theriogenology 24, 345–350.
Embryo transfer as a means of controlling viral infections. VI. Bluetongue virus-free calves from infectious semen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVymtw%3D%3D&md5=2cc494d1fc2f11aaa22b72260a7490e1CAS | 16726088PubMed |

Toussaint, J. F., Vandenbussche, F., Mast, J., De Meester, L., Goris, N., Van Dessel, W., Vanopdenbosche, E., Kerkhofs, P., De Clercq, K., Zientara, S., Sailleau, C., Czaplicki, G., Depoorter, G., and Dochy, J. M. (2006). Bluetongue in northern Europe. Vet. Rec. 159, 327.
Bluetongue in northern Europe.Crossref | GoogleScholarGoogle Scholar | 16950894PubMed |

Vanbinst, T., Vandenbussche, F., Dernelle, E., and De Clercq, K. (2010). A duplex real-time RT PCR for the detection of bluetongue virus in bovine semen. J. Virol. Methods 169, 162–168.
A duplex real-time RT PCR for the detection of bluetongue virus in bovine semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtV2gtrzO&md5=a99dceb58779173538cde5b87a91f430CAS | 20674609PubMed |

Vandaele, L., De Clercq, K., Van Campe, W., De Leeuw, I., and Van Soom, A. (2012). Bluetonge virus infection in cattle after transfer of bovine in vivo-derived embryos. Reprod. Fertil. Dev. 24, 168.
Bluetonge virus infection in cattle after transfer of bovine in vivo-derived embryos.Crossref | GoogleScholarGoogle Scholar |

van den Brom, R., Luttikholt, S. J., Lievaart-Peterson, K., Peperkamp, N. H., Mars, M. H., van der Poel, W. H., and Vellema, P. (2012). Epizootic of ovine congenital malformations associated with Schmallenberg virus infection. Tijdschr. Diergeneeskd. 137, 106–111.
| 1:STN:280:DC%2BC383ptV2luw%3D%3D&md5=7d63320ce567a75b76e8092a758831dbCAS | 22393844PubMed |

Van Der Poel, W. H. M., Parlevliet, J. M., Verstraten, E. R., Kooi, E. A., Hakze-Van Der Honing, R., and Stockhofe, N. (2014). Schmallenberg virus detection in bovine semen after experimental infection of bulls. Epidemiol. Infect. 142, 1495–1500.
Schmallenberg virus detection in bovine semen after experimental infection of bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXosVWjt7Y%3D&md5=e4ad89d1acbb9b13534bbc2b615a0630CAS |

van Maanen, C., van der Heijden, H., Wellenberg, G. J., Witteveen, G., Luttikholt, S., Bouwstra, R., Kooi, B., Vellema, P., Peperkamp, K., and Mars, J. (2012). Schmallenberg virus antibodies in bovine and ovine fetuses. Vet. Rec. 171, 299.
Schmallenberg virus antibodies in bovine and ovine fetuses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bhtlaksA%3D%3D&md5=7598b33bcb1461e9fdb317034ba750ddCAS | 22922706PubMed |

Verwoerd, D., and Erasmus, B. J. (2004). Bluetongue. In ‘Infectious Diseases of Livestock’, 2nd edn. (Eds J. A. Coetzer and R. C. Tustin.) pp. 1201–1220. (Oxford University Press: Cape Town.)

Wernike, K., Holsteg, M., Schirrmeier, H., Hoffmann, B., and Beer, M. (2014). Natural infection of pregnant cows with Schmallenberg virus: a follow-up study. PLoS ONE 9, e98223.
Natural infection of pregnant cows with Schmallenberg virus: a follow-up study.Crossref | GoogleScholarGoogle Scholar | 24853555PubMed |

Wouda, W., Roumen, M. P., Peperkamp, N. H., Vos, J. H., van Garderen, E., and Muskens, J. (2008). Hydranencephaly in calves following the bluetongue serotype 8 epidemic in The Netherlands. Vet. Rec. 162, 422–423.
Hydranencephaly in calves following the bluetongue serotype 8 epidemic in The Netherlands.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c3hslaitw%3D%3D&md5=21c185360452988e2aa8d429b15486bcCAS | 18375990PubMed |

Zientara, S., Sailleau, C., Dauphin, G., Roquier, C., Remond, M., Lebreton, F., Hammoumi, S., Dubois, E., Agier, C., Merle, G., and Breard, E. (2002). Identification of bluetongue virus serotype 2 (Corsican strain) by reverse-transcriptase PCR reaction analysis of segment 2 of the genome. Vet. Rec. 150, 598–601.
Identification of bluetongue virus serotype 2 (Corsican strain) by reverse-transcriptase PCR reaction analysis of segment 2 of the genome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383psF2qsA%3D%3D&md5=61c3afc9786c41bd9ed7085760937f56CAS | 12036242PubMed |