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Although the transfer of embryos is much less likely to result in disease transmission than the transport of live animals, the sanitary risks associated with embryo transfer continue to be the subject of both scientific investigations and adaptations of national and international legislation. Therefore, the implications are important for veterinary practitioners and livestock breeders. In vivo-derived and in vitro-produced embryos are widely used in cattle and embryos from other species, such as sheep, goats, pigs and horses, are also currently being transferred in fairly significant numbers. Bearing in mind the wide variety of embryos of different species and the correspondingly large number of viruses that are of concern, it is expedient at this time to look again at the importance of the zona pellucida (ZP) as a barrier against viruses and at the susceptibility or otherwise of embryonic cells to viral infection if ever they are exposed. For embryos with an intact ZP, viral infection of the embryo is unlikely to occur. However, the virus may stick to the ZP and, in this case, International Embryo Transfer Society (IETS) washing procedures in combination with trypsin treatment are mandatory. A caveat is the fact that currently more and more types of embryos are becoming available for transfer and scientific data cannot be extrapolated from one species to another. These topics are discussed in the present review.

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Early experiments suggested that scrapie transmission via sheep embryos was a possibility, and gave rise to much controversy. However, when account is taken of the complex genetic effects on ovine susceptibility to scrapie, and of the several different scrapie strains with different clinical and pathological effects, the overall conclusion now is that transmission of classical scrapie by embryo transfer is very unlikely if appropriate precautions are taken. Recent embryo transfer studies have confirmed this. Other studies in sheep have shown that from about the middle of pregnancy the placental trophoblast is liable to scrapie infection in genetically susceptible ewes if the fetus is also susceptible. Since the contrary is also true, use of resistant ewes as embryo recipients could add to the safety of the embryo transfer, at least for classical scrapie. There has been little recent research on scrapie transmission via semen in sheep, and, with hindsight, the early studies, though negative, were inadequate. There is scant information on scrapie transfer via goat semen or embryos, although one study did find that bovine spongiform encephalopathy (BSE) was not transmitted via goat embryos. In cattle it has been shown that, if appropriate precautions are taken, the risks of transmitting BSE via semen and in vivo-derived embryos are negligible, and this conclusion has gained worldwide acceptance. Research on TSE transmission via reproductive technologies in deer has not yet been done, but information on the pathogenesis and epidemiology of chronic wasting disease (CWD) of deer, and on transmission risks in other species, provides optimism that transmission of CWD via semen and embryos of deer is unlikely. The presence of TSE infectivity in blood and various other tissues of infected animals, particularly sheep, gives rise to concerns that certain biological products currently used in reproductive technologies, e.g. pituitary gonadotrophins for superovulation, and certain tissue and blood products used in semen and embryo transfer media, could carry TSE infectivity. Instruments such as laparoscopes used for insemination, and for collection and transfer of embryos, especially in small ruminants, are also a concern because effective decontamination can be very difficult.

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This scientific review was prompted by recent legislation to curtail the use of semen from potentially virus-infected bulls to produce embryos for import into the European Union. From studies in laboratory animals, humans and horses, it is apparent that viruses may sometimes attach to, or be integrated into, spermatozoa, although in domestic livestock, including cattle, this seems to be a rare phenomenon, and carriage of virus through the zona pellucida into the oocyte by fertilising sperm has never been described in these species. Four specific viruses; enzootic bovine leukosis (EBLV), bovine herpesvirus-1 (BoHV-1), bovine viral diarrhoea virus (BVDV) and bluetongue virus (BTV), all of which tend to cause subclinical infections in cattle, but which can occur in bovine semen, are examined with regard to the risks that use of infected semen might lead to production of infected embryos. With regard to in vivo-derived embryos, when internationally approved embryo processing protocols are used, the risks from EBLV- and BTV-infected semen are negligible, and the same is almost certainly true for semen infected with BoHV-1 if the embryos are also treated with trypsin. For BVDV, there is insufficient data on how the virus is carried in semen and how different BVDV strains can interact with sperm, oocytes and embryos. There is a potential, at least, that in vivo-derived embryos resulting from infected semen might carry BVDV, although field studies so far suggest that this is very unlikely. With regard to in vitro-produced embryos, use of semen infected with any of the four viruses, with the probable exception of EBLV, will often lead to contaminated embryos, and virus removal from these embryos is difficult even when the internationally approved embryo processing protocols are used. However, it has never been demonstrated that such embryos have resulted in transmission of infection to recipients or offspring.

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Semen from 13 bulls, eight with clinical bovine spongiform encephalopathy (BSE), was used to artificially inseminate (AI) 167 cows with clinical BSE, and their resultant embryos were collected non-surgically seven days after AI. The viable and non-viable embryos with intact zonae pellucidae were washed 10 times (as recommended by the International Embryo Transfer Society) then frozen. Later, 587 of the viable embryos were transferred singly into 347 recipient heifers imported from New Zealand, and 266 live offspring were born of which 54.1 per cent had a BSE-positive sire and a BSE-positive dam. The recipients were monitored for clinical signs of BSE for seven years after the transfer, and the offspring were monitored for seven years after birth. Twenty-seven of the recipients and 20 offspring died while being monitored but none showed signs of BSE. Their brains, and the brains of the recipients and offspring killed after seven years, were examined for BSE by histopathology, PrP immunohistochemistry, and by electron microscopy for scrapie-associated fibrils. They were all negative. In addition, 1020 non-viable embryos were sonicated and injected intracerebrally into susceptible mice (20 embryos per mouse) which were monitored for up to 700 days, after which their brains were examined for spongiform lesions. They were all negative. It is concluded that embryos are unlikely to carry BSE infectivity even if they have been collected at the end-stage of the disease, when the risk of maternal transmission is believed to be highest.

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Two-hundred-and-fifteen embryos recovered from 76 donor ewes from flocks endemically infected with sheep pulmonary adenomatosis (SPA) and mated with uninfected rams were transferred to 131 uninfected recipients under strict sanitary conditions using International Embryo Transfer Society protocols. The recipients and their progeny were kept in a closed, isolated SPA-free flock. Thirty-eight of 51 progeny from SPA-positive donors and 55 of 74 progeny from donors in which no lesions of SPA were detected survived for at least five years after birth. In a similar study 11 embryos from four uninfected donors mated to an SPA-infected ram were transferred to seven recipients, and four of five progeny born to four recipients survived for at least five years. No evidence of SPA was found in the recipients or their progeny by embryo transfer in either study. On the basis of clinical and pathological criteria, it is concluded that embryo transfer can be used to provide an effective barrier against the transmission of SPA from donors from infected flocks, whether or not the parents show clinical signs of the disease.

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This paper addresses the risks involved when bovine embryos are moved internationally and, specifically, the possibilities of transmitting foot-and-mouth disease, bluetongue and vesicular stomatitis by embryos originating from an area in South America. The risk scenario pathway was divided into three phases for analysis. The first phase dealt with the potential for embryo contamination which depends on the disease situation in the exporting country and/or region, the health status of the herds and the donor cows from which the embryos are collected, and the pathogenetic characteristics of the specified disease agent. The second phase covers risk mitigation by use of internationally accepted standards for processing of embryos, and the third phase encompassed the risk reductions resulting from post-collection surveillance of the donors and donor herds, and also from testing of embryo-collection (flushing) fluids for the disease agent. Quantitative risk analysis showed that under the circumstances specified in the paper, the risk of transmission of foot-and-mouth disease and vesicular stomatitis by embryos would be likely to be less than 1 in 100 billion (10(-11.0)) and 1 in 100 million (10(-8.0)), respectively. The values for bluetongue were 1 in 30,000 (10(-4.2)) when embryos were collected in the vector season and 1 in 1 million (10(-6.0)) in the season with low vector activity. These risk values were influenced by the incidence of each disease in the area of origin and the ease with which clinical signs can be recognised. Competent embryo processing according to procedures recommended by the International Embryo Transfer Society were also of great importance. The analysis showed that the reasons for the low levels of risk of transmission differed for each of the three diseases. In the case of bluetongue, vector ecology was of major importance.

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Guidelines for the safe international movement of livestock embryos are provided in the International Animal Health Code of the Office International des Epizooties, and recommendations for embryo processing, based on numerous research papers on embryo-pathogen interaction studies, are given in the Manual of the International Embryo Transfer Society. Risk assessment is the logical extension of these approaches, since it provides veterinary authorities with a complete package of information on which to base their import/export decisions. Risk assessment includes evaluation of disease prevalence, effectiveness of Veterinary Services and competence of the embryo collection team. It also takes account of the epidemiology and pathogenesis of the disease concerned. The application of risk assessment for embryo movement is illustrated in this paper by comparisons of the probabilities of transmitting foot and mouth disease, bluetongue and vesicular stomatitis by bovine embryos. The risk scenario pathway was divided into three phases for analysis. The first phase deals with the potential for embryo contamination, which depends on the disease situation in the exporting region, the health status of donor herds and donor cows, and on the pathogenetic properties of the disease agent. The second phase covers risk mitigation by use of the internationally accepted standards for embryo processing, and the third phase considers the risk reductions resulting from post-collection surveillance of donors and donor herds, and also from testing of embryo-collection (flushing) fluids for the disease agent. It was evident from this assessment that low risks of transmitting disease by international movement of bovine embryos depend initially on a low disease incidence in the exporting region and on easily recognisable disease signs. Competent embryo processing was also of great importance, and in the case of bluetongue, vector ecology had a major influence. In addition to providing a logical basis for import/export decisions, risk assessment is useful for evaluating the potential outcome of new research and for assessing the safety of the movement of embryos of other species for which little or no research information is available on embryo-pathogen interactions.

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This paper reviews current knowledge on transmission of scrapie and bovine spongiform encephalopathy (BSE) by semen and embryos. In sheep, in particular, it is difficult to distinguish between the genetic transmission of susceptibility to scrapie and vertical transmission of the infection. Nevertheless, there is evidence that vertical transmission of infection does occur, probably across the placenta, but none to suggest a significant scrapie risk from semen. Two teams have studied scrapie transmission from experimentally infected sheep using embryo transfer. Whereas one team found no evidence for transmission, the results from the other team suggest that embryos, even after washing, might carry the disease into the offspring. In regard to goats, although genetic differences in susceptibility exist, they are much less obvious than in sheep. There is no evidence for vertical transmission or for transmission through semen and embryos. With regard to BSE, although it appears that genetic differences in susceptibility are absent or unimportant, some recent work does suggest that the disease may be passed from cow to calf. The route of transmission and stage or stages when this takes place are unclear, however. In conclusion, despite growing evidence to indicate that scrapie and BSE are unlikely to be transmitted through semen and embryos, more research is needed to confirm this. Furthermore, until all possibility of risk is ruled out, risk reduction methods must be considered, especially when semen and embryos are being imported into countries where the diseases do not exist.

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[Introduction] The objective of Part I of this publication is the development of a QRA model for disease transmission by ET. Bovine ET was chosen for the discussions because bovine embryos are the most commonly used in international trade. In Part I, Section 1 some of the general aspects of bovine ET procedures are briefly reviewed, while Section 2 contains a general discussion of the risk factors involved. In Section 3 the scenario pathway is show and the general principles of risk quantification are outlined. Practical application of the QRA model is presented in Part II of the paper. This deals with the construction os a specific QRA model for the risk of transmission of FMD by bovine ET from a FMD infected country. Because of the important potential for export of embryos of Zebu cattle breeds from Brazil, particurlarly from the area comprising the model. Part II Section 1 gives some specific details of the epidemiology and conrol od FMD in the area concerned. The status of the ET industry of Brazil and in the selected area is also reviewed. In section 2 a quantification of the risks is proposed. Also, documentation is provided on the evidence and information used for the proposed risk values, followed by the statistical elaboration of the risk estimates, discussion and conclusions.

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A diagnosis of congenital goitre was confirmed histologically in piglets which were born hairless and swollen, and with significantly enlarged thyroid glands. The iodine content of the thyroid glands and the serum total thyroxine concentrations were very low. No evidence was found of iodine deficiency or significant goitrogenic activity in the diet fed to the sows. An investigation of the parentage of six affected litters revealed that they all had one or other of two boars as the sire, grandsire or great grandsire. The suspicion of an inherited disorder was confirmed when a test mating of a suspect carrier boar and sow resulted in the birth of two affected piglets. The ratio of the numbers of affected and unaffected piglets was statistically consistent with an autosomal recessive mode of inheritance.

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Until and including 1987 diagnostically significant serological titres to swine brucellosis had occurred in the serum agglutination test (SAT) or the complement fixation test (CFT), ie, > or = 100 iu or > or = 20 icftu, respectively, almost every year since reliable records began, but usually only about 0.05 per cent in the SAT and 0.005 per cent in the CFT. Brucella suis was never isolated by cultural examination. In 1988 the level of CFT reactions > or = 20 icftu rose to 0.42 per cent (1.04 per cent in the last quarter of the year) but the SAT reactions remained relatively unchanged. In 1989 the levels of both CFT and SAT reactions increased further with CFT reactions again predominating. Analyses of the serological reaction patterns in individual herds suggested that infection with brucella or some other organism capable of causing serological cross-reactions had become widespread in Great Britain, although signs of disease typical of swine brucellosis had not been observed. Some herds had reactions which persisted for many months whereas others showed them for only a short time. In early 1990 Yersinia enterocolitica serogroup O:9 was isolated from some pigs purchased from one of the reactor herds and this organism is probably responsible for the increased numbers of seroreactions. It had not previously been found in pigs in Great Britain.

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From the point of view of disease risk, the movement of livestock by embryo transfer is undoubtedly much safer for trading than the movement of live animals or semen. Nevertheless, strict governmental control by veterinary certification of health of embryos is still vital. In cattle, sheep and pigs, unlike laboratory species such as the mouse, infectious agents do not appear to pass through the zona pellucida (ZP) into the embryo proper. Some agents do, however, adhere firmly to the outer surface of the ZP, especially onto those of the pig. Disease risks associated with the inadvertent transmission of infectious agents when embryos are moved are, therefore, intimately connected with the nature and properties of the ZP. This article reviews current knowledge on the physical and adhesive properties of the ZP and discusses how risks associated with the possible presence of infection on its surface can be minimized. Further research is urgently needed so that realistic but safe veterinary certification of the health of embryos for international trade can be devised.

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Following intranasal exposure to PCMV at or within 48 h of coitus transplacental infection occurred in two groups of gilts. Five out of 22 embryos were infected in the first group but only 2 out of 63 in the second. A more rapid immune response as measured by circulating antibody was probably instrumental in abrogating infection in the second group. In the infected embryos the virus localized in leptomeningeal cells, hepatic sinusoidal cells, peritoneal macrophages, periosteal cells and occasional alveolar cells, but the placenta did not appear to be a primary site of viral replication.

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Inactivated porcine parvovirus vaccines have been available commercially in Britain since 1984 and are now widely used in breeding herds. To investigate their value in cost benefit terms an oil-emulsion vaccine developed at Weybridge was used in trials on 1243 gilts in 12 herds during the period 1984 to 1986. In each herd approximately half the gilts were given the vaccine before breeding and the remainder were left unvaccinated. Blood samples were taken at vaccination and two to four weeks later to measure the serological responses, and the reproductive performances of the two groups were compared. When the data from all the gilts in the 12 herds were combined and analysed together there was surprisingly little difference between the reproductive performance of the vaccinated and unvaccinated groups. Only when the results from individual herds were analysed and interpreted against a background knowledge of wild parvovirus activity (as derived from a study of the serological results) did an understanding and evaluation of the benefits of vaccination become possible. As herds vary with respect to the absence or presence of porcine parvovirus and the epidemiology of the infection it is recommended that vaccination be used with discrimination; it should then prove highly cost effective.

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Four sows with circulating antibody were exposed to porcine cytomegalovirus. Virus was detected in 8 of 24 foetuses by immunofluorescence and/or virus isolation from 2 sows with low levels of antibody. In 6 of the infected foetuses, the virus was in capillary endothelium and macrophages of the lung, and was associated with interlobular oedema in 2 of these. Virus was also detected in the nasal mucosa, spleen and brain. The majority of the virus-positive foetuses were grossly normal.

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Two sows which had been vaccinated with an oil-emulsion porcine parvovirus vaccine, and had developed high haemagglutination-inhibiting antibody levels to the virus, farrowed three successive litters each, a total of 74 piglets. Serum samples from these piglets were tested for haemagglutination-inhibiting antibody at birth, three and 17 days after birth, and at monthly intervals thereafter to study the decline of maternally-derived antibody. Regression curves were constructed from the data to show the projected pathway (mean and 95 per cent tolerance limits) of the decline of maternally-derived antibody. Approximately half the pigs still had positive titres of up to 1/160 at six months old, and traces of antibody were detected in a few pigs at nine months. Thus, even at the onset of breeding some gilts can have maternally-derived antibody which may interfere with their ability to develop active immunity to porcine parvovirus. From the same litters three groups of 12 pigs were selected randomly and were vaccinated with a single dose of the oil-emulsion vaccine at 70 days, 130 days or 190 days respectively. Despite the presence of moderate to high titres of maternally-derived antibody, especially in the younger pigs, all of those vaccinated showed strong and long lasting antibody responses to the vaccine. High serum antibody titres at the time of vaccination seemed to depress the response to the vaccine slightly but the effect was not statistically significant. These results have important implications for prevention of reproductive failure induced by porcine parvovirus.

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Three inactivated porcine parvovirus vaccines were tested for efficacy in 66 susceptible gilts. The gilts were challenged with virulent virus on the 40th day of gestation. All the vaccines provided excellent protection against fetal mortality despite insignificant serological responses to one of them. Good protection was obtained with two of the vaccines even when the dose was substantially reduced. Unvaccinated controls had very few viable fetuses.

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