Biosecurity issues associated with current and emerging embryo technologies
David A. Stringfellow A B , M. Daniel Givens A and Julie G. Waldrop A
+ Author Affiliations
- Author Affiliations
A College of Veterinary Medicine, Auburn University, AL 36849-5519, USA.
B To whom correspondence should be addressed. email: strinda@vetmed.auburn.edu
Reproduction, Fertility and Development 16(2) 93-102 https://doi.org/10.1071/RD03082
Submitted: 1 August 2003 Accepted: 1 October 2003 Published: 2 January 2004
Abstract
A variety of procedures associated with in vivo and in vitro embryo production, as well as cloning and transgenics, are in current use by both researchers and practitioners. Biohazards associated with these procedures could influence clinical proficiency and the outcome of basic research or result in unusual distribution of pathogens in populations of animals. By their nature, embryo technologies are vulnerable to contamination from numerous sources. Although pathogens can originate in the physical environments in which embryo technologies are applied, they are more likely to be introduced via animals or materials of animal origin. However, it is important to note that both the occurrence and consequences of contamination are heavily influenced by environmental circumstances. This paper represents a philosophical description of biohazards associated with three generations of embryo technologies using the cow as a model species. Emphasis is placed on sources of contamination, current or suggested preventive actions and the issue of environmental changes as they relate to the emergence of biohazards and the implementation of biosecurity measures. Some specific pathogens are discussed for illustration. In addition, details of the risks associated with introducing bovine viral diarrhoea virus in each of three generations of embryo technologies are described.
Extra keywords: biohazard, bovine viral diarrhea virus (BVDV), embryo–pathogen interactions.
References
Anonymous, (1996).
Anonymous, (2003).
Anderson, M. L. , Andrianarivo, A. G. , and Conrad, P. A. (2000). Neosporosis in cattle. Anim. Reprod. Sci. 60–61, 417–432.
| Crossref | GoogleScholarGoogle Scholar |
Avery, B. , Greve, T. , Ronsholt, L. , and Botner, A. (1993). Virus screening of a bovine in vitro embryo production system. Vet. Rec. 132, 660.
| PubMed |
Bak, A. , Callesen, H. , Meyling, A. , and Greve, T. (1992). Calves born after embryo transfer from donors persistently infected with BVD virus. Vet. Rec. 131, 37.
| PubMed |
Baker, J. C. (1987). Bovine viral diarrhea virus: a review. J. Am. Vet. Med. Assoc. 190, 1449–1458.
| PubMed |
Betteridge, K. J. (2000). Reflections on the golden anniversary of the first embryo transfer to produce a calf. Theriogenology 53, 3–10.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bielanski, A. (1997). A review on disease transmission studies in relationship to production of embryos by in vitro fertilization and to related new reproductive technologies. Biotechnol. Adv. 15, 633–656.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bielanski, A. , and Dubuc, C. (1995). In vitro fertilization of ova from cows experimentally infected with a noncytopathic strain of bovine viral diarrhea virus. Anim. Reprod. Sci. 38, 215–222.
| Crossref | GoogleScholarGoogle Scholar |
Bielanski, A. and Hare, W. C. D. (1998). Procedures for design and analysis of research on transmission of infectious disease by embryo transfer. In
Bielanski, A. , and Jordan, L. (1996). Washing or washing and trypsin treatment is ineffective for removal of noncytopathic bovine viral diarrhea virus from bovine oocytes or embryos after experimental viral contamination of an in vitro fertilization system. Theriogenology 46, 1467–1476.
| Crossref | GoogleScholarGoogle Scholar |
Bielanski, A. , and Stewart, B. (1996). Ubiquitous microbes isolated from in vitro fertilization (IVF) system. Theriogenology 45, 269.
| Crossref | GoogleScholarGoogle Scholar |
Bielanski, A. , and Surujballi, O. (1998). Leptospira borgpetersenii serovar hardjo type hardjobovis in bovine embryos fertilized in vitro. Can. J. Vet. Res. 62, 234–236.
| PubMed |
Bielanski, A. , Loewen, K. S. , Del Campo, M. R. , Sirard, M. A. , and Willadsen, S. (1993). Isolation of bovine herpesvirus-1 (BHV-1) and bovine viral diarrhea virus (BVDV) in association with the in vitro production of bovine embryos. Theriogenology 40, 531–538.
| Crossref | GoogleScholarGoogle Scholar |
Bielanski, A. , Sampath, M. , Gradil, C. , Eaglesome, M. D. , and Garcia, M. (1994). In vitro fertilization of bovine ova in the presence of Campylobacter fetus subsp. venerealis. Reprod. Domest. Anim. 29, 488–493.
Bolin, S. R. , and Ridpath, J. F. (1998). Prevalence of bovine viral diarrhea virus genotypes and antibody against those viral genotypes in fetal bovine serum. J. Vet. Diagn. Invest. 10, 135–139.
| PubMed |
Booth, P. J. , Stevens, D. A. , Collins, M. E. , and Brownlie, J. (1995). Detection of bovine viral diarrhea virus antigen and RNA in oviduct and granulosa cells of persistently infected cattle. J. Reprod. Fertil. 105, 17–24.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brock, K. V. (1998). Quality controls for materials of animal origin used in embryo production and transfer. In
Brock, K. V. , Lapin, D. R. , and Skrade, D. R. (1997). Embryo transfer from donor cattle persistently infected with bovine viral diarrhea virus. Theriogenology 47, 837–844.
| Crossref | GoogleScholarGoogle Scholar |
Brownlie, J. (1990). The pathogenesis of bovine viral diarrhea virus infections. Rev. Sci. Tech. Off. Int. Epiz. 9, 43–59.
Cohn, E. J. , Strong, L. E. , Hughes, W. L. , Mulford, D. J. , Ashworth, J. N. , Melin, M. , and Taylor, H. L. (1946). Preparation and properties of serum and plasma proteins. IV. A system for the separation into fractions of the protein and lipoprotein components of biological tissues and fluids. J. Am. Chem. Soc. 68, 459–475.
Drew, T. W. , Sandrik, T. , Wakeley, P. , Jones, T. , and Howard, P. (2002). BVD virus genotype 2 detected in British cattle. Vet. Rec. 151, 551.
Dinkin, 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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Edens, M. S. D. , Galik, P. K. , Riddell, K. P. , Givens, M. D. , Stringfellow, D. A. , and Loskutoff, N. M. (2002). Bovine herpesvirus-1 associated with single, trypsin-treated embryos is not infective for uterine tubal cells. Theriogenology 57, 570.(Abstract)
Engels, M. , and Ackermann, M. (1996). Pathogenesis of ruminant herpesvirus infections. Vet. Microbiol. 53, 3–15.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fray, M. D. , Prentice, H. , Clarke, M. C. , and Charleston, B. (1998). Immunohistochemical evidence for localization of bovine viral diarrhea virus, a single-stranded RNA virus, in ovarian oocytes in the cow. Vet. Pathol. 35, 253–259.
| PubMed |
Fray, M. D. , Paton, D. J. , and Alenius, S. (2000). The effects of bovine viral diarrhea virus on cattle reproduction in relation to disease control. Anim. Reprod. Sci. 60–61, 615–627.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Galli, C. , Duchi, R. , Crotti, G. , Turini, P. , Ponderato, N. , Colleoni, S. , Lagutina, I. , and Lazzari, G. (2003). Bovine embryo technologies. Theriogenology 59, 599–616.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Givens, M. D. , Galik, P. K. , Riddell, K. P. , Brock, K. V. , and Stringfellow, D. A. (1999a). 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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Givens, M. D. , Galik, P. K. , Riddell, K. P. , and Stringfellow, D. A. (1999b). Uterine tubal cells remain uninfected after culture with in vitro-produced embryos exposed to bovine viral diarrhea virus. Vet. Microbiol. 70, 7–20.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Givens, M. D. , Galik, P. K. , Riddell, K. P. , Brock, K. V. , and Stringfellow, D. A. (2000). Replication and persistence of different strains of bovine viral diarrhea virus in an in vitro embryo production system. Theriogenology 54, 1093–1107.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Givens, M. D. , Galik, P. K. , Riddell, K. P. , Stringfellow, D. A. , Brock, K. V. , Bishop, M. D. , Eilertsen, K. J. , and Loskutoff, N. M. (2001). Validation of a reverse transcription nested polymerase chain reaction (RT-nPCR) to detect bovine viral diarrhea virus (BVDV) associated with in vitro-derived bovine embryos and co-cultured cells. Theriogenology 56, 787–799.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Givens, M. D. , Galik, P. K. , Riddell, K. P. , Stringfellow, D. A. , Dykstra, C. C. , Brock, K. V. , Kumar, A. , and Boykin, D. W. (2002). Aromatic cationic molecules inhibit replication of bovine viral diarrhea virus but not development of IVF embryos. Theriogenology 57, 572.(Abstract)
Givens, M. D. , Dykstra, C. C. , Brock, K. V. , Stringfellow, D. A. , Kumac, A. , Stephens, C. E. , Goker, H. , and Boykin, D. W. (2003a). Detection of inhibition of bovine viral diarrhea virus by aromatic cationic molecules. Antimicrob. Agents Chemother. 47, 2223–2230.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Givens, M. D. , Stringfellow, D. A. , Riddell, K. P. , Galik, P. K. , Carson, R. L. , Riddell, M. G. , Dykstra, C. C. , and Boykin, D. W. (2003b). Pregnancies established after treatment of IVF bovine embryos with an antiviral agent. Theriogenology 59, 382.(Abstract)
Gordon, I. (1994).
Guerin, B. , Chaffaux, St. , Marquant-Le Guienne, B. , Allietta, M. , and Thibier, M. (1992). IVF and IV culture of bovine embryos using semen from a bull persistently infected with BVDV. Theriogenology 37, 217.(Abstract)
| Crossref | GoogleScholarGoogle Scholar |
Guerin, B. , Nibart, M. , Marquant-Le Guienne, B. , and Humblot, P. (1997). Sanitary risks related to embryo transfer. Theriogenology 47, 33–42.
| Crossref | GoogleScholarGoogle Scholar |
Hare, W. C. D. (1985). Status of disease transmission studies and their relationship to the international movement of bovine embryos. Can. Vet. J. 27, 37–45.
Houe, H. (1999). Epidemiological features and economic importance of bovine viral diarrhea virus. Vet. Microbiol. 64, 89–107.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lindberg, A., Ortman, K. and Alenius, S. (2000). Seroconversion to bovine viral diarrhea virus (BVDV) in dairy heifers after embryo transfer. In
Mapletoft, R. J. (1986). Bovine embryo transfer. In
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marquant-Le Guienne, B. , Delalleau, N. , Halay, T. , Allietta, M. , Diemert, S. , Le Tallec, B. , and Guerin, B. (2000). Results of a four-year survey on viral and bacterial contamination in a bovine in vitro embryo production system when using slaughterhouse material. Theriogenology 53, 321.
Nettleton, P. and Vilcek, S. (2001). Detection of pestiviruses in bovine serum. In
Nibart, M., Marquant-Le Guienne, B. and Humblot, P. (1998). General sanitary procedures associated with in-vitro production of embryos. In
Riddell, K. P. and Stringfellow, D. A. (1998). The use of antibiotics in media for recovery, culture, and storage of embryos. In
Ridpath, J. F. , Bolin, S. R. , and Dubovi, E. J. (1994). Segregation of bovine viral diarrhea virus into genotypes. Virology 205, 66–74.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| PubMed |
Schiewe, M. (1998). General hygiene and quality control practices in an embryo production laboratory. In
Shin, T. , Sneed, L. , Hill, J. R. , and Westhusin, M. E. (2000). High incidence of developmental failure in bovine fetuses derived by cloning bovine viral diarrhea virus-infected cells. Theriogenology 53, 243.
Singh, E. L. (1987). The disease control potential of embryos. Theriogenology 27, 9–20.
| Crossref | GoogleScholarGoogle Scholar |
Singh, E. L. , Eaglesome, M. D. , Thomas, F. C. , Papp-Vid, G. , and Hare, W. C. D. (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.
| Crossref | GoogleScholarGoogle Scholar |
Smith, A. K. , and Grimmer, S. P. (2000). Birth of a BVDV-free calf from a persistently infected embryo transfer donor. Vet. Rec. 146, 49–50.
| PubMed |
Smith, R. D. (1995).
Stringfellow, D. A. (1985). The potential of bovine embryo transfer for infectious disease control. Rev. Sci. Tech. Off. Int. Epiz. 4, 859–866.
Stringfellow, D. A. (1998). Recommendations for the sanitary handling of in vivo-derived embryos. In
Stringfellow, D. A. (2002). Use of materials of animal origin in embryo production schemes: continued caution is recommended. Embryo Transfer Newsletter 20, 11.
Stringfellow, D. A. , and Givens, M. D. (2000a). Epidemiologic concerns relative to in vivo and in vitro production of livestock embryos. Anim. Reprod. Sci. 60–61, 629–642.
| Crossref | GoogleScholarGoogle Scholar |
Stringfellow, D. A. , and Givens, M. D. (2000b). Infectious agents in bovine embryo production: hazards and solutions. Theriogenology 53, 85–94.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stringfellow, D. A. , Riddell, K. P. , and Zurovac, O. (1991). The potential of embryo transfer for infectious disease control in livestock. N. Z. Vet. J. 39, 8–17.
Stringfellow, J. S. , Hathcock, T. L. , Riddell, K. P. , Stringfellow, D. A. , Galik, P. K. , Riddell, M. G. , and Carson, R. L. (1997). Introduction of Stenotrophomonas maltophilia through semen used for in vitro production of bovine embryos. Theriogenology 47, 382.(Abstract)
| 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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| PubMed |
Thibier, M. (1990). New biotechnologies in cattle production. In
Trachte, E. , Stringfellow, D. , Riddell, K. , Galik, P. , Riddell, M. , and Wright, J. (1998). Washing and trypsin treatment of in vitro derived embryos exposed to bovine viral diarrhea virus. Theriogenology 50, 717–726.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vanroose, G. , Nanwynek, H. , Vansoom, A. , Vanopdenbosch, E. , and De Kruif, A. (1999). Effects of bovine herpesvirus-1 or bovine viral diarrhea virus on development of in vitro-produced bovine embryos. Mol. Reprod. Dev. 54, 255–263.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vanroose, G. , Nauwynek, H. , Vansoom, A. , Ysebaert, M. T. , Charlier, G. , Van Oostueldt, P. , and De Kruif, A. (2000). Structural aspects of the zona pellucida of in vitro-produced bovine embryos: a scanning electron and confocal laser scanning microscopic study. Biol. Reprod. 62, 463–469.(Abstract)
| PubMed |
Waldrop, J. G. , Stringfellow, D. A. , Givens, M. D. , Riddell, K. P. , Galik, P. K. , Riddell, M. G. , Carson, R. L. , and Brock, K. V. (2002). Association of bovine viral diarrhea virus (BVDV) with artificially exposed, in vivo-derived, bovine embryos varies between different viral strains. Theriogenology 57, 575.
Wentink, G. H. , Aarts, T. , Mirck, M. H. , and van Exsel, A. C. A. (1991). Calf from a persistently infected heifer born after transfer with normal immunity to BVDV. Vet. Rec. 129, 449–450.
| PubMed |
Westhusin, M. E. , Long, C. R. , Shin, T. , Hill, J. R. , Looney, C. R. , Pryor, J. H. , and Piedrahita, J. A. (2001). Cloning to reproduce desired genotypes. Theriogenology 55, 35–49.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wrathall, A. E. (1997). Risk of transmitting scrapie and bovine spongiform encephalopathy by semen and embryos. Rev. Sci. Tech. Off. Int. Epiz. 16, 240–264.
Wrathall, A. E. (2000). Risks of transmission of spongiform encephalopathies by reproductive technologies in domesticated ruminants. Livest. Prod. Sci. 62, 287–316.
| Crossref | GoogleScholarGoogle Scholar |
Wrathall, A. E. and Sutmoller, P. (1998). Potential of embryo transfer to control transmission of disease. In
Wrathall, A. E. , Brown, K. F. D. , Sayers, A. R. , Wells, G. A. H. , and Simmons, M. M. , et al. (2002). Studies of embryo transfer from cattle clinically affected by bovine spongiform encephalopathy (BSE). Vet. Rec. 150, 365–378.
| PubMed |
