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

Emerging diseases in international trade in embryos

Julie Gard Schnuelle
+ Author Affiliations
- Author Affiliations

Department of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL 36849-5522, USA. Email: waldrja@auburn.edu

Reproduction, Fertility and Development 33(2) 55-65 https://doi.org/10.1071/RD20207
Published: 8 January 2021

Abstract

A significant change in cattle production and germplasm exchange has occurred over the past 50 years. The growth of artificial reproductive technologies and their broad implementation has become commonplace. The production and subsequent import and export of semen and embryos throughout the world has increased significantly. The embryo transfer industry has reached a new record of growth, with approximately 1.5 million transferrable bovine embryos collected and/or produced in 2018. Over 1 million of these embryos were produced in vitro. The increased production of in vitro-produced embryos leads to greater opportunities involving international trade. However, further research concerning emerging pathogens is imperative to ensure the efficacy and safety of the embryo transfer industry. Appropriate biosecurity protocols, including reliable testing methodology and effective embryo processing procedures, are key in preventing disease due to emerging and re-emerging pathogens that can be transmitted via embryo transfer.

Keywords: embryo pathogens, embryo transfer, in vitro-produced embryos, in vivo-derived embryos.


References

Adams, D. B. (2016). Prenatal transmission of scrapie in sheep and goats: a case study for veterinary public health. Open Vet. J. 6, 194–214.
Prenatal transmission of scrapie in sheep and goats: a case study for veterinary public health.Crossref | GoogleScholarGoogle Scholar | 27928518PubMed |

Andréoletti, O., Orge, L., Benestad, S. L., Beringue, V., Litaise, C., Simon, S., Le, D. A., Laude, H., Simmons, H., Lugan, S., Corbière, F., Costes, P., Morel, N., Schelcher, F., and Lacroux, C. (2011). Atypical/Nor98 scrapie infectivity in sheep peripheral tissues. PLoS Pathogens 7, e1001285.
Atypical/Nor98 scrapie infectivity in sheep peripheral tissues.Crossref | GoogleScholarGoogle Scholar | 21445238PubMed |

Anonymous (2019a) Chapter 4.9. Terresterial Animal Health Code, 28th edition, of the World Organization for Animal Health (OIE). Available at https://www.oie.int/index.php?id=169&L=0&htmfile=chapitre_coll_embryo_invitro.htm [Verified 2 September 2020]

Anonymous (2019b) Chapter 1.11. Terresterial Animal Health Code, 28th edition, of the World Organization for Animal Health (OIE). Available at https://www.oie.int/index.php?id=169&L=0&htmfile=chapitre_selfdeclaration_FMD.htm [Verified 2 September 2020].

Anonymous (2019c) Chapter 4.8.14 Terresterial Animal Health Code, 28th edition, of the World Organization for Animal Health (OIE). Available at https://www.oie.int/index.php?id=169&L=0&htmfile=chapitre_coll_embryo_equid.htm [Verified 2 September 2020].

Asseged, B. D., Habtemariam, T., Tameru, B., and Nganwa, D. (2012). The risk of introduction of equine infectious anemia virus into USA via cloned horse embryos imported from Canada. Theriogenology 77, 445–458.
The risk of introduction of equine infectious anemia virus into USA via cloned horse embryos imported from Canada.Crossref | GoogleScholarGoogle Scholar | 21958631PubMed |

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 | 19419822PubMed |

Bauermann, F. V., Ridpath, J. F., Weiblen, R., and Flores, E. F. (2013). HoBi-like viruses: an emerging group of pestiviruses. J. Vet. Diagn. Invest. 25, 6–15.
HoBi-like viruses: an emerging group of pestiviruses.Crossref | GoogleScholarGoogle Scholar | 23345268PubMed |

Bielanski, A. (2009). Risk of contamination of germ plasm during cryopreservation and cryobanking. In ‘Manual of the International Embryo Transfer Society’. 4th edn. (Eds D. A. Stringfellow and M. D. Givens.) pp. 131–140. (IETS: Savoy, IL.)

Bielanski, A., and Dubuc, C. (1995). in vitro fertilization of ova from cows experimentally infected with a non-cytopathic strain of bovine viral diarrhea virus. Anim. Reprod. Sci. 38, 215–221.
in vitro fertilization of ova from cows experimentally infected with a non-cytopathic strain of bovine viral diarrhea virus.Crossref | GoogleScholarGoogle Scholar |

Bielanski, A., and Jordan, L. (1996). Washing or washing and trypsin treatment is ineffective for removal of non-cytopathic bovine viral diarrhea virus from bovine oocytes or embryos after experimental viral contamination of an in vitro fertilization system. Theriogenology 46, 1467–1476.
Washing or washing and trypsin treatment is ineffective for removal of non-cytopathic bovine viral diarrhea virus from bovine oocytes or embryos after experimental viral contamination of an in vitro fertilization system.Crossref | GoogleScholarGoogle Scholar |

Bielanski, A., and Lalonde, A. (2009). Effect of cryopreservation by slow cooling and vitrification on viral contamination of IVF embryos experimentally exposed to bovine viral diarrhea virus and bovine herpesvirus-1. Theriogenology 72, 919–925.
Effect of cryopreservation by slow cooling and vitrification on viral contamination of IVF embryos experimentally exposed to bovine viral diarrhea virus and bovine herpesvirus-1.Crossref | GoogleScholarGoogle Scholar | 19616294PubMed |

Bielanski, A., and Vaita, G. (2009). Risk of contamination of germplasm during cryopreservation and cryobanking in IVF units. Hum. Reprod. 24, 2457–2467.
Risk of contamination of germplasm during cryopreservation and cryobanking in IVF units.Crossref | GoogleScholarGoogle Scholar | 19561041PubMed |

Bielanski, A., Eaglesome, M. D., Ruhnke, H. L., and Hare, W. C. D. (1989). Isolation of Mycoplasma bovis from intact and microinjected preimplantation bovine embryos washed and treated with trypsin or antibiotics. J. in Vitro Fert. Embryo Transf. 6, 236–241.
Isolation of Mycoplasma bovis from intact and microinjected preimplantation bovine embryos washed and treated with trypsin or antibiotics.Crossref | GoogleScholarGoogle Scholar | 2614219PubMed |

Bielanski, A., Sapp, T., and Lutze-Wallace, C. (1998a). Association of bovine embryos produced by in vitro fertilization with a noncytopathic strain of BVDV type II. Theriogenology 49, 1231–1238.
Association of bovine embryos produced by in vitro fertilization with a noncytopathic strain of BVDV type II.Crossref | GoogleScholarGoogle Scholar | 10732060PubMed |

Bielanski, A., Normando, S., Lutze-Wallace, C., Sapp, T., Gardioli, P., and Luini, M. (1998b). Treatment of oocytes and in vitro fertilized embryos with monoclonal antibodies and guinea pig complement for neutralization of contaminating bovine herpesvirus-1. Reprod. Domest. Anim. 33, 89–92.
Treatment of oocytes and in vitro fertilized embryos with monoclonal antibodies and guinea pig complement for neutralization of contaminating bovine herpesvirus-1.Crossref | GoogleScholarGoogle Scholar |

Bielanski, A., Algire, J., Lalonde, A., and Nadin-Davis, S. (2009). Transmission of bovine viral diarrhea virus (BVDV) via in vitro-fertilized embryos to recipients, but not to their offspring. Theriogenology 71, 499–508.
Transmission of bovine viral diarrhea virus (BVDV) via in vitro-fertilized embryos to recipients, but not to their offspring.Crossref | GoogleScholarGoogle Scholar | 18834622PubMed |

Booth, P. J., Collins, M. E., Jenner, L., Prentice, H., Ross, J., Badsberg, J. H., and Brownlie, J. (1998). Noncytopathic bovine viral diarrhea virus (BVDV) reduces cleavage but increases blastocyst yield of in vitro produced embryos. Theriogenology 50, 769–777.
Noncytopathic bovine viral diarrhea virus (BVDV) reduces cleavage but increases blastocyst yield of in vitro produced embryos.Crossref | GoogleScholarGoogle Scholar | 10734451PubMed |

da Silva Cardoso Pinto, V., Alves, M. F., de Souza Nunes Martinsa, M., Basso, A. C., Tannura, J. H., Pontes, J. H. F., Santos Lima, M., Garcia da Silva, T., Okuda, L. H., Stefano, E., Romaldini, A. H. C. N., Arnold, D. R., and Pituco, E. M. (2017). Effects of oocytes exposure to bovine diarrhea viruses BVDV-1, BVDV-2 and Hobi-like virus on in vitro-produced bovine embryo development and viral infection. Theriogenology 97, 67–72.
Effects of oocytes exposure to bovine diarrhea viruses BVDV-1, BVDV-2 and Hobi-like virus on in vitro-produced bovine embryo development and viral infection.Crossref | GoogleScholarGoogle Scholar | 28583610PubMed |

Detwiler, L. A., and Baylis, M. (2003). The epidemiology of scrapie. Rev. Sci. Tech. 22, 121–143.
The epidemiology of scrapie.Crossref | GoogleScholarGoogle Scholar | 12793776PubMed |

Dinkins, M. B., Stallknecht, D. E., and Brackett, B. G. (2001). Reduction of infectious epizootic hemorrhagic disease virus associated with in vitro-produced bovine embryos by non-specific protease. Anim. Reprod. Sci. 65, 205–213.
Reduction of infectious epizootic hemorrhagic disease virus associated with in vitro-produced bovine embryos by non-specific protease.Crossref | GoogleScholarGoogle Scholar | 11267800PubMed |

Engels, M., and Ackermann, M. (1996). Pathogenesis of ruminant herpesvirus infections. Vet. Microbiol. 53, 3–15.
Pathogenesis of ruminant herpesvirus infections.Crossref | GoogleScholarGoogle Scholar | 9010994PubMed |

Fediaevsky, A., Morigna, E., Ducrot, C., and Calavas, D. (2009). A case-control study on the origin of atypical scrapie in sheep, France. Emerg. Infect. Dis. 15, 710–718.
A case-control study on the origin of atypical scrapie in sheep, France.Crossref | GoogleScholarGoogle Scholar | 19402956PubMed |

Fediaevsky, A., Gasqui, P., Calavas, D., and Ducrot, C. (2010). Discrepant epidemiological patterns between classical and atypical scrapie in sheep flocks under French TSE control measures. Vet. J. 185, 338–340.
Discrepant epidemiological patterns between classical and atypical scrapie in sheep flocks under French TSE control measures.Crossref | GoogleScholarGoogle Scholar | 19635675PubMed |

Flores, E. F., Cargnelutti, J. F., Monteiro, F. L., Bauermann, F. V., Ridpath, J. F., and Weiblen, R. A. (2018). Genetic profile of bovine pestiviruses circulating in Brazil (1998–2018). Anim. Health Res. Rev. 19, 134–141.
Genetic profile of bovine pestiviruses circulating in Brazil (1998–2018).Crossref | GoogleScholarGoogle Scholar | 30683172PubMed |

Galik, P. K., Givens, M. D., Stringfellow, D. A., Crichton, E. G., Bishop, M. D., and Eilertsen, K. J. (2002). Bovine viral diarrhea virus (BVDV) and anti-BVDV antibodies in pooled samples of follicular fluid. Theriogenology 57, 1219–1227.
Bovine viral diarrhea virus (BVDV) and anti-BVDV antibodies in pooled samples of follicular fluid.Crossref | GoogleScholarGoogle Scholar | 12013443PubMed |

Galik, P. K., Gard, J. A., Spencer, T. S., Marley, M. S., Stringfellow, D. A., Givens, M. D., and Edmondson, M. A. (2008). Effects of ovine interferon-β on replication of bovine viral diarrhea virus and bovine herpesvirus-1. Reprod. Fertil. Dev. 20, 156–157.
Effects of ovine interferon-β on replication of bovine viral diarrhea virus and bovine herpesvirus-1.Crossref | GoogleScholarGoogle Scholar |

Gard, J. A (2015). Research challenges involving embryo pathogen interactions. Anim. Reprod. 12, 444–449.

Gard, J. A., and Stringfellow, D. A. (2014). Shaping the norms that regulate international commerce of embryos. Theriogenology 81, 56–66.
Shaping the norms that regulate international commerce of embryos.Crossref | GoogleScholarGoogle Scholar | 24274410PubMed |

Gard, J. A., Givens, M. D., and Stringfellow, D. A. (2007). Bovine viral diarrhea virus (BVDV): epidemiologic concerns relative to semen and embryos. Theriogenology 68, 434–442.
Bovine viral diarrhea virus (BVDV): epidemiologic concerns relative to semen and embryos.Crossref | GoogleScholarGoogle Scholar | 17588651PubMed |

Gard, J. A., Givens, M. D., Marley, M. S. D., Galik, P. K., Riddell, K. P., Edmondson, M. A., and Rodning, S. P. (2010). Intrauterine inoculation of seronegative heifers with bovine viral diarrhea virus simultaneous to transfer of in vivo-derived bovine embryos. Theriogenology 73, 1009–1017.
Intrauterine inoculation of seronegative heifers with bovine viral diarrhea virus simultaneous to transfer of in vivo-derived bovine embryos.Crossref | GoogleScholarGoogle Scholar | 20129656PubMed |

Garza, M. C., Fernández-Borges, N., Bolea, R., Badiola, J. J., Castilla, J., and Monleón, E. (2011). Detection of PrPres in genetically susceptible fetuses from sheep with natural scrapie. PLoS One 6, e27525.
Detection of PrPres in genetically susceptible fetuses from sheep with natural scrapie.Crossref | GoogleScholarGoogle Scholar | 22194786PubMed |

Givens, M. D., and Marley, M. S. D. (2008). Infectious causes of embryonic and fetal mortality. Theriogenology 70, 270–285.
Infectious causes of embryonic and fetal mortality.Crossref | GoogleScholarGoogle Scholar | 18502494PubMed |

Givens, M. D., Galik, P. K., Riddell, K. P., Brock, K. V., and Stringfellow, D. A. (1999). Quantity and infectivity of embryo-associated bovine viral diarrhea virus and antiviral influence of a blastocyst impede in vitro infection of uterine tubal cells. Theriogenology 52, 887–900.
Quantity and infectivity of embryo-associated bovine viral diarrhea virus and antiviral influence of a blastocyst impede in vitro infection of uterine tubal cells.Crossref | GoogleScholarGoogle Scholar | 10735128PubMed |

Givens, M. D., Stringfellow, D. A., Dykstra, C. C., Riddell, K. P., Galik, P. K., Sullivan, E., Robl, J., Kasinathan, P., Kumar, A., and Boykin, D. W. (2004). Prevention and elimination of bovine viral diarrhea virus infections in fetal fibroblast cells. Antiviral Res. 64, 113–118.
Prevention and elimination of bovine viral diarrhea virus infections in fetal fibroblast cells.Crossref | GoogleScholarGoogle Scholar | 15498606PubMed |

Givens, M. D., Stringfellow, D. A., Riddell, K. P., Galik, P. K., Carson, R. L., Riddell, M. G., and Navarre, C. B. (2006). Normal calves produced after transfer of in vitro fertilized embryos cultured with an antiviral compound. Theriogenology 65, 344–355.
Normal calves produced after transfer of in vitro fertilized embryos cultured with an antiviral compound.Crossref | GoogleScholarGoogle Scholar | 15955552PubMed |

Haapalaa, V., Pohjanvirtab, T., Vähänikkiläb, N., Halkilahtic, J., Simonend, H., Pelkonenb, S., Soveria, T., Simojokia, H., and Autiob, T. (2018). Semen as a source of Mycoplasma bovis mastitis in dairy herds. Vet. Microbiol. 216, 60–66.
Semen as a source of Mycoplasma bovis mastitis in dairy herds.Crossref | GoogleScholarGoogle Scholar |

Haegeman, A., Vandaele, L., De Leeuw, I., Oliveira, A. P., Nauwynck, H., Van Soom, A., and DeClercq, K. (2019). Failure to remove bluetongue serotype 8 virus (BTV-8) from in vitro produced and in vivo derived bovine embryos and subsequent transmission of BTV-8 to recipient cows after embryo transfer. Front. Vet. Sci. 6, 432.
Failure to remove bluetongue serotype 8 virus (BTV-8) from in vitro produced and in vivo derived bovine embryos and subsequent transmission of BTV-8 to recipient cows after embryo transfer.Crossref | GoogleScholarGoogle Scholar | 31867345PubMed |

Hercík, K., Kozak, J., Sala, M., Dejmek, M., Hrebabecky, H., Zbornikova, E., Smola, M., Ruzek, D., Nencka, R., and Boura, E. (2017). Adenosine triphosphate analogs can efficiently inhibit the Zika virus RNA-dependent RNA polymerase. Antiviral Res. 137, 131–133.
Adenosine triphosphate analogs can efficiently inhibit the Zika virus RNA-dependent RNA polymerase.Crossref | GoogleScholarGoogle Scholar | 27902932PubMed |

Hopp, P., Omer, M. K., and Heier, B. T. (2006). A case-control study of scrapie Nor98 in Norwegian sheep flocks. J. Gen. Virol. 87, 3729–3736.
A case-control study of scrapie Nor98 in Norwegian sheep flocks.Crossref | GoogleScholarGoogle Scholar | 17098991PubMed |

Houe, H. (1999). Epidemiological features and economical importance of bovine virus diarrhea virus (BVDV) infections. Vet. Microbiol. 64, 89–107.
Epidemiological features and economical importance of bovine virus diarrhea virus (BVDV) infections.Crossref | GoogleScholarGoogle Scholar | 10028165PubMed |

Kohara, J., Nishikura, Y., Konnai, S., Tajima, M., and Onuma, M. (2012). Effects of interferon-tau on cattle persistently infected with bovine viral diarrhea virus. Jpn. J. Vet. Res. 60, 63–70.
| 23094581PubMed |

Lamara, A., Fieni, F., Mselli-Lakhal, L., Chatagnon, G., Bruyas, J. F., Tainturier, D., Battut, I., Fornazero, C., and Chebloune, Y. (2002). Early embryonic cells from in vivo-produced goat embryos transmit the caprine arthritis-encephalitis virus (CAEV). Theriogenology 58, 1153–1163.
Early embryonic cells from in vivo-produced goat embryos transmit the caprine arthritis-encephalitis virus (CAEV).Crossref | GoogleScholarGoogle Scholar | 12240918PubMed |

Ligios, C., Cancedda, M. G., Carta, A., Santucciu, C., Maestrale, C., Demontis, F., Saba, M., Patta, C., DeMartini, J. C., Aguzzi, A., and Sigurdson, C. J. (2011). Sheep with scrapie and mastitis transmit infectious prions through the milk. J. Virol. 85, 1136–1139.
Sheep with scrapie and mastitis transmit infectious prions through the milk.Crossref | GoogleScholarGoogle Scholar | 21084475PubMed |

Marquant-Le Guienne, B., Remond, M., Cosquer, R., Humblot, P., Kaiser, C., Lebreton, F., Cruciere, C., Guerin, B., LaPorte, J., and Thibier, M. (1998). Exposure of in vitro-produced embryos to foot-and-mouth disease virus. Theriogenology 50, 109–116.
Exposure of in vitro-produced embryos to foot-and-mouth disease virus.Crossref | GoogleScholarGoogle Scholar |

Menzies, F. D., McCullough, S. J., McKeown, I. M., Forster, J. L., Jess, S., Batten, C., Murchie, A. K., Gloster, J., Fallows, J. G., Pelgrim, W., Mellor, P. S., and Oura, C. A. L. (2008). Evidence for transplacental and contact transmission of bluetongue in cattle. Vet. Rec. 163, 203–209.
Evidence for transplacental and contact transmission of bluetongue in cattle.Crossref | GoogleScholarGoogle Scholar | 18708653PubMed |

Read, A. J., Gestier, S., Parrish, K., Finlaison, D. S., Gu, X., O’Connor, T. W., and Kirkland, P. D. (2020). Prolonged detection of bovine viral diarrhoea virus infection in the semen of bulls. Viruses 12, 674.
Prolonged detection of bovine viral diarrhoea virus infection in the semen of bulls.Crossref | GoogleScholarGoogle Scholar |

Newcomer, B. W., Marley, M. S., Ridpath, J. F., Neil, J. D., Boykin, D. W., Kumar, A., and Givens, M. D. (2012). Efficacy of an antiviral compound to inhibit replication of multiple pestivirus species. Antiviral Res. 96, 127–129.
Efficacy of an antiviral compound to inhibit replication of multiple pestivirus species.Crossref | GoogleScholarGoogle Scholar | 22985628PubMed |

Newcomer, B. W., Walz, P. H., Givens, M. D., and Wilson, A. E. (2015). Efficacy of bovine viral diarrhea virus vaccination to prevent reproductive disease: a meta-analysis. Theriogenology 83, 360–365.e1.
Efficacy of bovine viral diarrhea virus vaccination to prevent reproductive disease: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 25447148PubMed |

Newcomer, B. W., Grady Cofield, L., Walz, P. H., and Givens, M. D. (2017). Prevention of abortion in cattle following vaccination against bovine herpesvirus 1: a meta-analysis. Prev. Vet. Med. 138, 1–8.
Prevention of abortion in cattle following vaccination against bovine herpesvirus 1: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 28237224PubMed |

Nicholson, E. M., Brunelle, B. W., Richt, J. A., Kehrli, M. E., and Greenlee, J. J. (2008). Identification of a heritable polymorphism in bovine PRNP associated with genetic transmissible spongiform encephalopathy: evidence of heritable BSE. PLoS One 3, e2912.
Identification of a heritable polymorphism in bovine PRNP associated with genetic transmissible spongiform encephalopathy: evidence of heritable BSE.Crossref | GoogleScholarGoogle Scholar | 18698343PubMed |

Nims, R. W., Gauvin, G., and Plavsic, M. (2011). Gamma irradiation of animal sera for inactivation of viruses and mollicutes – a review. Biologicals 39, 370–377.
Gamma irradiation of animal sera for inactivation of viruses and mollicutes – a review.Crossref | GoogleScholarGoogle Scholar | 21871817PubMed |

OIE (2019) Terresterial Animal Health Code, 28th Edition, of the World Organization for Animal Health (OIE). Available at https://www.oie.int/standard-setting/terrestrial-code/access-online/ [Verified 9 October 2020].

Perry, G. H. (2007). Risk assessment of transmission of bovine viral diarrhea virus (BVDV) in abattoir-derived in vitro produced embryos. Theriogenology 68, 38–55.
Risk assessment of transmission of bovine viral diarrhea virus (BVDV) in abattoir-derived in vitro produced embryos.Crossref | GoogleScholarGoogle Scholar | 17462725PubMed |

Pinheiro de Oliveira, T. F., Fonseca, A. A., Camargos, M. F., de Oliveira, A. M., Cottorello, A. C. P., dos Reis Souza, A., de Almeida, L. G., and Heinemann, M. B. (2013). Detection of contaminants in cell cultures, sera and trypsin. Biologicals 41, 407–414.
Detection of contaminants in cell cultures, sera and trypsin.Crossref | GoogleScholarGoogle Scholar | 24071554PubMed |

Riddell, K. P., Stringfellow, D. A., Gray, B. W., Riddell, M. G., and Galik, P. K. (1993). Antibiotic treatment of bovine embryos. J. Assist. Reprod. Genet. 10, 488–491.
Antibiotic treatment of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 8069094PubMed |

Ridpath, J. F. (2008). Bovine viral diarrhea virus. In ‘Encyclopedia of Virology’. 3rd edn. (Eds B. W. J. Mahy and M. H. V. Van Regenmortel.) pp. 374–380. (Academic Press Inc.)

Rossi, C. R., Bridgman, R. S., and Kiesel, G. K. (1980). Viral contamination of bovine fetal lung cultures and bovine fetal serum. Am. J. Vet. Res. 41, 1680–1681.
| 6261615PubMed |

Rubenstein, R., Bulgin, M. S., Chang, B., Sorensen-Melson, S., Petersen, R. B., and LaFauci, G. (2012). PrPSc detection and infectivity in semen from scrapie-infected sheep. J. Gen. Virol. 93, 1375–1383.
PrPSc detection and infectivity in semen from scrapie-infected sheep.Crossref | GoogleScholarGoogle Scholar | 22323531PubMed |

Silva-Frade, C., Martins, A., Borsanelli, A. C., and Cardoso, T. C. (2010a). Effects of bovine herpesvirus type 5 on development of in vitro-produced bovine embryos. Theriogenology 73, 324–331.
Effects of bovine herpesvirus type 5 on development of in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 19896706PubMed |

Silva-Frade, C., Gameiro, R., Martins, A., and Cardoso, T. C. (2010b). Apoptotic and developmental effects of bovine herpesvirus type-5 infection on in vitro-produced bovine embryos. Theriogenology 74, 1296–1303.
Apoptotic and developmental effects of bovine herpesvirus type-5 infection on in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 20688374PubMed |

Song, B. S., Kim, J. S., Yoon, S. B., Lee, K. S., Koo, D. B., Lee, D. S., Choo, Y. K., Huh, J. W., Lee, S. R., Kim, S. U., Kim, S. H., Kim, H. M., and Chang, K. T. (2011). Inactivated Sendai-virus-mediated fusion improves early development of cloned bovine embryos by avoiding endoplasmic-reticulum-stress-associated apoptosis. Reprod. Fertil. Dev. 23, 826–836.
Inactivated Sendai-virus-mediated fusion improves early development of cloned bovine embryos by avoiding endoplasmic-reticulum-stress-associated apoptosis.Crossref | GoogleScholarGoogle Scholar | 21791184PubMed |

Spera, A. M., Eldin, T. K., Tosone, G., and Orlando, R. (2016). Antiviral therapy for hepatitis C: has anything changed for pregnant/lactating women? World J. Hepatol. 8, 557–565.
Antiviral therapy for hepatitis C: has anything changed for pregnant/lactating women?Crossref | GoogleScholarGoogle Scholar | 27134703PubMed |

Stringfellow, D. A. (2009). Recommendations for the sanitary handling of in-vivo-derived embryos. In ‘Manual of the International Embryo Transfer Society’. 4th edn. (Eds D. A. Stringfellow and M. D. Givens.) pp. 65–68. (IETS: Savoy, IL.)

Stringfellow, D. A., and Givens, M. D. (2000). Preventing disease transmission through the transfer of in-vivo-derived bovine embryos. Livest. Prod. Sci. 62, 237–251.
Preventing disease transmission through the transfer of in-vivo-derived bovine embryos.Crossref | GoogleScholarGoogle Scholar |

Stringfellow, D. A., Riddell, K. P., Galik, P. K., Damiani, P., Bishop, M. D., and Wright, J. C (2000). Quality controls for bovine viral diarrhea virus-free IVF embryos. Theriogenology 53, 827–839.
Quality controls for bovine viral diarrhea virus-free IVF embryos.Crossref | GoogleScholarGoogle Scholar | 10735047PubMed |

Stringfellow, D. A., Givens, M. D., and Waldrop, J. G. (2004). Biosecurity issues associated with current and emerging embryo technologies. Reprod. Fertil. Dev. 16, 93–102.
Biosecurity issues associated with current and emerging embryo technologies.Crossref | GoogleScholarGoogle Scholar | 14972107PubMed |

Stringfellow, D. A., Riddell, K. P., Givens, M. D., Galik, P. K., Sullivan, E., Dykstra, C. C., Robl, J., and Kasinathan, P. (2005). Bovine viral diarrhea virus (BVDV) in cell lines used for somatic cell cloning. Theriogenology 63, 1004–1013.
Bovine viral diarrhea virus (BVDV) in cell lines used for somatic cell cloning.Crossref | GoogleScholarGoogle Scholar | 15710188PubMed |

Sweeney, R. W., Whitlock, R. H., and Rosenberger, A. E. (1992). Mycobacterium paratuberculosis isolated from fetuses of infected cows not manifesting signs of disease. Am. J. Vet. Res. 53, 477–480.
| 1586015PubMed |

Thibier, M., and Stringfellow, D. (2003). Health and Safety Advisory Committee (HASAC) of the International Embryo Transfer Society (IETS) has managed critical challenges for two decades. Theriogenology 59, 1067–1078.
Health and Safety Advisory Committee (HASAC) of the International Embryo Transfer Society (IETS) has managed critical challenges for two decades.Crossref | GoogleScholarGoogle Scholar | 12517404PubMed |

Trachte, E., Stringfellow, D. A., Riddell, K. P., Galik, P. K., Riddell, M. G., and Wright, J. (1998). Washing and trypsin treatment of in vitro derived bovine embryos exposed to bovine viral diarrhea virus. Theriogenology 50, 717–726.
Washing and trypsin treatment of in vitro derived bovine embryos exposed to bovine viral diarrhea virus.Crossref | GoogleScholarGoogle Scholar | 10734446PubMed |

Vähänikkilä, N., Pohjanvirta, T., Haapala, V., Simojoki, H., Soveri, T., Browning, G. F., Pelkonen, S., Wawegama, N. K., and Autio, T. (2019). Characterisation of the course of Mycoplasma bovis infection in naturally infected dairy herd. Vet. Microbiol. 231, 107–115.
Characterisation of the course of Mycoplasma bovis infection in naturally infected dairy herd.Crossref | GoogleScholarGoogle Scholar | 30955796PubMed |

Vanroose, G., Naunwynek, H., Van Soom, A., Vanopdenbosch, E., and DeKruif, A. (1999). Effects of bovine herpesvirus-1 on bovine viral diarrhea virus on development of in vitro-produced bovine embryos. Mol. Reprod. Dev. 54, 255–263.
Effects of bovine herpesvirus-1 on bovine viral diarrhea virus on development of in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 10497347PubMed |

Vanroose, G., Nauwynek, H., Van Soom, H., Ysebarert, M. T., Charlier, G., Van Oostveldt, P., and de Kruif, A. (2000). Structural aspects of the zona pellucida of in-vitro-produced embryos: a scanning electron and confocal laser scanning microscopic study. Biol. Reprod. 62, 463–469.
Structural aspects of the zona pellucida of in-vitro-produced embryos: a scanning electron and confocal laser scanning microscopic study.Crossref | GoogleScholarGoogle Scholar | 10642588PubMed |

Viana, J. (2019). Statistics of embryo production and transfer in domestic farm animals. Embyro Technol. Newsl. 36, 7–29. Available at https://www.iets.org/pdf/Newsletter/Dec19_IETS_Newsletter.pdf [Verified 2 September 2020].

Waldrop, J. G., Stringfellow, D. A., Riddell, K. P., Galik, P. K., Riddell, M. G., Givens, M. D., Carson, R. L., and Brock, K. V. (2004). Different strains of noncytopathic bovine viral diarrhea virus (BVDV) vary in their affinity for in vivo-derived bovine embryos. Theriogenology 62, 45–55.
Different strains of noncytopathic bovine viral diarrhea virus (BVDV) vary in their affinity for in vivo-derived bovine embryos.Crossref | GoogleScholarGoogle Scholar | 15159100PubMed |

Waldrop, J. G., Stringfellow, D. A., Galik, P. K., Givens, M. D., Riddell, K. P., Riddell, M. G., and Carson, R. L. (2006). Seroconversion of calves following intravenous injection with embryos exposed to bovine viral diarrhea virus (BVDV) in vitro. Theriogenology 65, 594–605.
Seroconversion of calves following intravenous injection with embryos exposed to bovine viral diarrhea virus (BVDV) in vitro.Crossref | GoogleScholarGoogle Scholar | 16039701PubMed |

Whittington, R. J., and Windsor, P. A. (2009). In utero infection of cattle with Mycobacterium avium subsp. paratuberculosis: a critical review and meta-analysis. Vet. J. 179, 60–69.
In utero infection of cattle with Mycobacterium avium subsp. paratuberculosis: a critical review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 17928247PubMed |

World Organisation for Animal Health (OIE) (2019). Section 4. Disease prevention and control. In ‘Terresterial Animal Health Code’. 28th edn. Availablhttps://www.oie.int/standard-setting/terrestrial-code/access-online/ [verified 02, 09, 2020.

Wrathall, A. E. (2000). Risks of transmission of spongiform encephalopathies by reproductive technologies in domesticated ruminants. Livest. Prod. Sci. 62, 287–316.
Risks of transmission of spongiform encephalopathies by reproductive technologies in domesticated ruminants.Crossref | GoogleScholarGoogle Scholar |

Wrathall, A. E., Brown, K. F. D., Sayers, A. R., Wells, G. A. H., Simmons, M. M., Farrelly, S. S. J., Bellerby, P., Squirrell, J., Spencer, Y. I., Wells, M., Stack, M. J., Bastiman, B., Pullar, D., Scatchers, J., Heasman, L., Parker, J., Hannam, D. A. R., Helliwell, D. W., Chree, A., and Fraser, H. (2002). Studies of embryo transfer from cattle clinically affected by bovine spongiform encephalopathy (BSE). Vet. Rec. 150, 365–378.
Studies of embryo transfer from cattle clinically affected by bovine spongiform encephalopathy (BSE).Crossref | GoogleScholarGoogle Scholar | 11936410PubMed |

Wrathall, A. E., Simmons, H. A., and Van Soom, A. (2006). Evaluation of risks of viral transmission to recipients of bovine embryos arising from fertilization with virus-infected semen. Theriogenology 65, 247–274.
Evaluation of risks of viral transmission to recipients of bovine embryos arising from fertilization with virus-infected semen.Crossref | GoogleScholarGoogle Scholar | 16005506PubMed |

Wrathall, A. E., Ayling, R. D., and Simmons, H. A. (2007). Risks of transmitting mycoplasmas by semen and embryo transfer techniques in cattle, sheep, goats and pigs. Perspect. Agric. Vet. Sci. Nutr. Nat. Resour. 2, 1–31.
Risks of transmitting mycoplasmas by semen and embryo transfer techniques in cattle, sheep, goats and pigs.Crossref | GoogleScholarGoogle Scholar |

Wrathall, A. E., Holyoak, G. R., Parsonson, I. M., and Simmons, H. A. (2008). Risks of transmitting ruminant spongiform encephalopathies (prion diseases) by semen and embryo transfer techniques. Theriogenology 70, 725–745.
Risks of transmitting ruminant spongiform encephalopathies (prion diseases) by semen and embryo transfer techniques.Crossref | GoogleScholarGoogle Scholar | 18586320PubMed |