Prevalence of BoHV-1 seropositive and BVD virus positive bulls on Irish dairy farms and associations between bull purchase and herd status

Artificial insemination (AI) has become the breeding norm on the majority of dairy farms in the Republic of Ireland [1]. However, the stock bull (a bull used for breeding purposes) also remains an integral part of the breeding process on many farms, either being relied on as a sole means of impregnating cows or as an adjunct to AI later in the breeding season [2]. Milk production systems in Ireland are primarily pasture-based and involve seasonal calving [3]. Over 80 % of Irish dairy farms are spring-calving with the majority of cows calving down in the first 6 months of the year and 21 % of all calves are born in March alone [4]. Compact spring-calving is essential to the efficiency of farms which operate extensive grass-based systems as calving is timed to coincide with the period of maximal grass growth [3]. Calves born later in the year will reduce farm efficiency [5].

A key breeding goal in a spring-calving system is to achieve high 3 and 6-week pregnancy rates from breeding start date to achieve a concentrated calving pattern the next season [6]. Bulls can be an efficient means of getting cows in calf as the breeding season progresses and also reduce the need for continuing heat detection [2]. Use of 6 weeks of AI followed by release of bulls to complete the breeding season is, therefore, a common reproductive strategy on many Irish dairy farms [1]. For the purposes of genetic diversity, these bulls are often purchased and are only introduced to the female breeding herd during the breeding season. Ensuring the health of these bulls is of paramount importance, therefore, in terms of bull fertility and disease transmission between cows and bulls. Bovine Viral Diarrhoea (BVD) and Infectious Bovine Rhinotracheitis (IBR) caused by BVD virus (BVDv) and bovine herpesvirus 1 (BoHV-1), respectively, are highly contagious diseases of economic and trade importance. Both are listed as notifiable diseases by the World Organisation for Animal Health (OIE) and are prevalent in Ireland [7]. Several European countries have implemented programmes to eradicate both diseases to facilitate free trade of cattle, semen, and embryos within the European Union (EU). Ireland embarked on a compulsory national eradication programme for BVD in 2013 based on identification of BVD persistently infected (PI) calves. Movement restrictions are placed on individuals testing BVD virus positive [8]. As of yet, no regulation exists for control and eradication of BoHV-1.

Cattle movement has been explored by many authors as a root cause of disease spread [9, 10]. Many Irish farmers operate what they perceive as closed herds i.e. no cattle introductions to the farm [7]. It has previously been highlighted, however, that discrepancies exist between what Irish dairy farmers perceive as a closed herd and a herd that does not engage in purchase of any cattle [7]. Bulls are often an ‘overlooked’ purchase in the maintenance of a closed herd. Breeding bulls, as with any purchased animal [9], are capable of introducing disease to a farm and may act as a vehicle through which diseases such as BVD and BoHV-1 can be transmitted. BVD and BoHV-1 can both adversely affect the fertility on a dairy farm with potentially devastating consequences for achieving a compact breeding season [11–14].

The levels of BVD and BoHV-1 infection amongst dairy stock bulls in Ireland have never been examined nor has the degree of bull movement between farms. Therefore, the objectives of this study were (i) to provide descriptive, observational data on the use of stock bulls on Irish dairy farms; (ii) to investigate the BVD and BoHV1 status of a sub-set of stock bulls; (iii) to investigate factors associated with BVD and BoHV1 status of stock bulls and (iv) to investigate factors associated with dairy herd status for BVD and BoHV1, including any associations with the use of stock bulls.

BVD and BoHV-1 are contagious viral diseases of cattle and highly prevalent in Ireland (16). Although there are a number of studies carried out in beef and dairy cattle, it would appear that no studies have been carried out to investigate the degree of infection in the stock bull population. Despite the economic advantages of artificial insemination (AI) over natural service (NS), a high number of dairy farmers in Ireland that still rely on NS, compared to other European countries [18]. Among the participating farms in the current study, 77 % had at least one bull involved in the breeding process, whereas in Northern Europe, Israel or Japan, 80 to 90 % of dairy farmers use AI almost exclusively for breeding cattle [18].

A number of countries have reported BVD PI prevalence of between 0.4 and 1.1 %. The prevalence of PIs amongst Irish calves ear-notched as part of the national BVD eradication scheme in 2013 was 0.68 %², which has fallen to 0.46 % in 2014 and 0.32 % in 2015. It was not that surprising therefore, that two bulls out of 529 tested were positive for BVD virus in the current study. On reporting of initial BVDv results, the two study farmers involved elected to cull the virus positive animals without re-test to confirm PI status. The presence of clinical signs consistent with mucosal disease was identified in one bull (a purchased bull), the history of the second (a homebred ill-thrifty calf with recurring clinical issues), the low Ct values on PCR, and the absence of BVD antibodies, would suggest that both were BVD PIs [19]. PI animals are the main source of circulating BVDv leading to rapid secondary transmission once introduced to a herd. Bulls are also likely to be in very close contact with cows during the first trimester of pregnancy, and therefore may have a disproportionate impact on the generation of new PI animals the following year [20]. It is important in countries not yet engaging in BVD eradication, therefore, to monitor the breeding bull population as a potential source of BVDv.

It is also of note that one of the BVDv positive bulls identified was vasectomized. This bull was homebred, underweight and ill-thrifty as a calf, and could therefore not be sold at an early age with herd cohorts. The calf was therefore maintained on the farm and subsequently vasectomized, highlighting the ease with which a PI can be maintained on farm and may ultimately contribute to the breeding process on a dairy farm. Based on these results, the use of vasectomized bulls and choice of animal to be vasectomized deserves careful consideration on dairy farms. Vasectomized bulls act as a cost-saving measure for heat detection purposes [21], but if the animal is not chosen carefully, the long term economic consequences can easily outweigh any benefit. The importance of ensuring the absence of PI animals on a farm cannot be overstated.

Based on the results of the current study, the likelihood of introducing of BoHV-1 seropositive bull would appear greater than BVDv positive bulls. While a previous Irish study reported 6 % of beef bulls selected for performance testing by the national cattle breeding centre as being seropositive for BoHV-1 [22], just over 16 % of dairy bulls in the current study were positive. No difference between dairy and beef herds in terms of BoHV-1 was reported previously [23]. The difference in bull prevalence recorded may reflect differences in age groups investigated as a much older cohort of animals were included in the current study. A number of studies have reported older animals to be more likely to be seropositive for BoHV-1 [9, 24, 25], which is in agreement with the results obtained in this study.

Purchased bulls were three times more likely to be BoHV-1 seropositive in the current study. Cattle trade and movement, in general, have been reported by a number of authors as major risk factors for the spread of BoHV-1 [9, 26, 27]. The number of movements recorded for individual bulls in this study was remarkable and an unsurprising trend was highlighted whereby the more ‘between-farm’ movements recorded by a particular bull, the higher the likelihood of being BoHV-1 seropositive. This may be due to the higher number of risk interactions (shows, markets, transport) that these bulls experience. This aligns with results from previous surveys [27] which recorded a higher predisposition of BoHV-1 seropositive herds to buy cattle and participate in shows. These results highlight the importance of seeking a full diagnostic and movement history prior to purchasing a breeding bull. These findings should be considered in other jurisdictions where stock bulls remain an important part of the breeding programme.

An additional noteworthy finding of this study was the significant association between purchase of bulls with both BVD herd status and BoHV-1 viral circulation. The high probability of having recent BoHV-1 viral circulation in herds that purchased bulls has also been identified in previous studies [9], where purchase of cattle (as opposed to just stock bulls) identified as a major direct risk factor for BoHV-1 infection. It was not possible in the current study to obtain records of additional purchased cattle on study farms as individual identifiers for other cattle were not available. This is a potential weakness of the study, as purchase of a bull may be a proxy for purchase of additional high risk cattle onto a farm. It has been reported previously that bulls are more likely to be seropositive than cows [9], making them a higher risk purchase and further investigation is required to more clearly highlight the contribution of stock bulls to disease introduction on dairy farms. Nevertheless, this study has highlighted a clear association between purchase of bulls and an undesirable BVD and BoHV-1 status.

Farms with non-homebred bulls were three times more likely to be bulk milk positive for BVD than those farms where all the bulls were homebred, in contrast to BoHV-1, where no relationship was found. This most likely relates to the differences in the dynamic of spread of both viruses across a herd population. In the case of BoHV-1, a large proportion of latent carriers exist within an adult dairy herd allowing for the possibility of continuing re-infection from within the herd itself. In contrast to this, transmission of BVDv in the adult herd is dependent on contact with a PI. Many PIs die, however, before reaching breeding age [28], leading to a break in re-infection. The culling rate of dairy cows in Ireland (25 %) [29], coupled to death of PIs at a young age, may lead to dairy herds having more cyclical BVDv transmission rather than the continuous re-infection possible in unvaccinated BoHV-1 infected dairy herds. The contribution of a purchased infected bull, therefore, in increasing the bulk milk antibody levels in a herd, is most likely greater for BVDv. Regardless of the differences in associations detected between BVDv and BoHV-1, these results again support the hypothesis that introducing purchased bulls in the farm could led to an increased risk for both viral infections.

Two factors were significantly associated with an increased BoHV-1 herd serostatus. This included farm location and the number of bulls present on each farm. Farms in Region 1 (lower cattle density) had a higher probability of being positive for BoHV-1, which has already been investigated by other authors [16], who propose that it could be due to the higher proportion of beef cattle in the region and a reduced probability of implementing biosecurity measures. The association between number of stock bulls and BoHV-1 herd seropositivity is a novel finding. Considering that bulls are more at risk of being seropositive than cows [9] and that once the virus is introduced in the herd the infection is quickly disseminated amongst herd mates [30]; the higher number of bulls maintained in the farm could lead to a higher risk of BoHV-1 infection. Again this highlights the potential role of stock bulls in viral disease dissemination on farm making them a cohort of animals that should undergo disease screening prior to movement or purchase.

Minimal attention has been dedicated internationally to the role of stock bulls in transmission of infectious diseases in dairy farms. This study recorded widespread use of stock bulls on Irish dairy farms, a high degree of ‘between-farm’ movement of these animals, and the potential for bulls to act as a vector of disease between farms. Further studies into the role of stock bulls in transmission of viral diseases, in countries where NS is common practice, is required, as is the role of these breeding animals in transmission of other infectious pathogens.