Definition and causal agent

Bovine viral diarrhea virus (BVDV) has a worldwide distribution and affects cattle of all breeds and ages (OIE, 2017). BVDV belongs to the Pestivirus genus of the Flaviviridae family (Simmonds et al., Reference Simmonds, Becher, Collet, Gould, Heinz, Meyers, Monath, Pletnev, Rice, Stiansny, Thiel, Weiner, Bukhet, King, Adams, Carstens and Lefkowitz2011). Two main genotypes have been described: BVDV-1 and BVDV-2, which have been classified as separate species in the Pestivirus genus. Europe is mainly dominated by BVDV-1, while there is an equal prevalence of BVDV-1 and BVDV-2 in North America (Lindberg et al., Reference Lindberg, Berriatua, Fourichon, Mintiens and Houe2006a).

Both genotypes are classified into the two distinct biotypes: cytopathic and non-cytopathic (Ridpath and Bolin, Reference Ridpath and Bolin1998), according to the different type of proteins coded from their genomic RNA (Neill, Reference Neill2013). A third genotype has also now been identified (OIE, 2017).

BVD is one of the most serious infectious diseases of cattle, leading to severe economic losses to the cattle industry and, as such, it is one of the most studied bovine diseases (Gunn et al., Reference Gunn, Stott and Humphry2004). BVDV results in a number of complex clinical manifestations in cattle. Clinical syndromes associated with the reproductive system are particularly damaging, resulting in significant economic losses due to abortions and perinatal mortality in affected animals. A serious aspect of the reproductive syndrome is the birth of persistently infected (PI) calves. PI animals are the main reservoir of the virus and are the leading source of BVDV transmission. In addition, they can go on to develop fatal mucosal disease (Bianchi et al., Reference Bianchi, Konradt, de Souza, Bassuino, Silveira, Mosena, Canal, Pavarini and Driemeier2017). BVDV also results in enteritis during acute or transient infection, which although generally not severe, can occasionally be fatal even in adult animals. Transient infection is believed to cause immunosuppression and is likely to contribute to bovine respiratory disease (BRD) (OIE, 2017). Given the wide variety of clinical manifestations resulting from BVDV infection, comprehensive knowledge of the signs and symptoms at each stage of the disease is essential for its management and control.

Transmission

BVDV transmission can be direct, with the main routes of infection being ingestion or inhalation of the virus (Grooms et al., Reference Grooms, Baker, Ames and Smith2014). It is transmitted through contact with saliva, oculonasal discharge, uterine secretions, amniotic fluid or placenta, semen, urine and feces from PI animals or acutely infected animals (Newcomer et al., Reference Newcomer, Chamorro and Walz2017). As the virus is able to cross the placental barrier, vertical transmission can occur between pregnant females and their fetuses (Grooms et al., Reference Grooms, Baker, Ames and Smith2014). BVDV transmission can also be indirect, through vectors such as hematophagous insects, needles and surgical equipment, etc. (Grooms et al., Reference Grooms, Baker, Ames and Smith2014).

It has been found that BVDV can survive in slurry for up to 3 weeks at 5°C (Bøtner and Belsham, Reference Bøtner and Belsham2012). However, it is believed that the virus generally cannot survive more than 14 days in the environment and is likely susceptible to a range of common disinfectants such as hypochlorite, iodophors and chlorhexidine (Bøtner and Belsham, Reference Bøtner and Belsham2012).

Vaccination

There are several factors to be considered when incorporating the use of vaccines in BVD control. The first factor is whether to use modified live viral (MLV) vaccines or inactivated vaccines. Choosing a suitable biotype, BVDV-1 or BVDV-2, and genotype and subtype are also key considerations. In addition, it is important to evaluate if the formulation will be monovalent or multivalent (Newcomer et al., Reference Newcomer, Chamorro and Walz2017).

Inactivated BVDV vaccines, while safer than live vaccines, have variable effectiveness due to their low immunogenicity, which is directly correlated with antigenic concentration (Fernández et al., Reference Fernández, Costantini, Barrandeguy, Parreño, Schiappacassi, Maliandi, Leunda and Odeón2009). Furthermore, because they are produced with less diversity of strains, they offer reduced cross-protection. BVDV vaccines are frequently combined with other reproductive and respiratory complex pathogens, meaning that they offer less BVDV viral antigen, and can lead to the development of low levels of antibodies by the host, providing inadequate immune protection against BVDV (Pecora et al., Reference Pecora, Malacari, Pérez Aguirreburualde, Bellido, Escribano, Dus Santos and Wigdorovitz2015). In addition, the emergence of bovine neonatal pancytopenia, a fatal disease associated with the use of inactivated BVD vaccines, has been reported in a number of European countries, including Scotland (Bell et al., Reference Bell, Scott, Sargison, Wilson, Morrison, Howie, Willoughby and Penny2010; Pecora et al., Reference Pecora, Malacari, Pérez Aguirreburualde, Bellido, Escribano, Dus Santos and Wigdorovitz2015).

MLV vaccines have been approved in many countries and are frequently used in the European Union (EU) (Moennig and Brownlie, Reference Moennig and Brownlie2006). Compared with inactivated vaccines, MLV vaccines produced a better immune response in the host, conferring greater protection (Woolums et al., Reference Woolums, Berghaus, Berghaus, Ellis, Pence, Saliki, Hurley, Galland, Burdett, Nordstrom and Hurley2013). However, they are less safe due to the possible risk of mutation, reactivation, and replication of the virus and the consequences that come with such events. As such, there are a number of countries where MLV vaccines have not yet been approved, including Argentina (Fernández et al., Reference Fernández, Costantini, Barrandeguy, Parreño, Schiappacassi, Maliandi, Leunda and Odeón2009).

Key considerations that must be kept at the forefront of any vaccination program include:

• • The safety of the vaccine and the levels of protection it confers.

• • The antigen diversity and strain diversity, taking into account the strains of BVDV present in the region (Jones et al., Reference Jones, Zandomeni and Weber2001).

• • Continuing surveillance to identify and characterize emerging BVDV field strains to appropriately reformulate vaccines (Fernández et al., Reference Fernández, Costantini, Barrandeguy, Parreño, Schiappacassi, Maliandi, Leunda and Odeón2009).

• • The timing of vaccination to fit with the farm's management plan and type of production (Newcomer et al., Reference Newcomer, Chamorro and Walz2017).

• • Design of programs that aim to reduce the birth of PI calves (Odeón, Reference Odeón2016).

Vaccination can make a significant contribution to the control of BVDV. Notwithstanding, it is significantly more effective when used alongside other biosecurity measures to prevent the introduction and circulation of the virus in herds (Newcomer et al., Reference Newcomer, Chamorro and Walz2017). It is important to highlight that vaccination is not compulsory in most countries (Jones et al., Reference Jones, Zandomeni and Weber2001) and is considered a useful complimentary biosecurity measure in BVDV control. However, with the development of safer and more effective vaccines, vaccination may come to play an even more important role in the future of BVDV control.

Overview of Scottish farming

Almost 80% of Scotland's total land area is under agricultural production, and income from agriculture constituted of approximately 1% of the Scottish economy in 2016 (Scottish Government, 2016a). While only 1% of Scotland's land is capable of producing a wide range of crops, in contrast, up to 48% can be used for grazing or rough grazing (Scottish Executive, 2001). As such, livestock accounts for almost 40% of total farm output, an estimated £1.11 billion, with 65% of this coming from cattle (Scottish Government, 2016a). Cattle farming is therefore an important aspect of the Scottish agricultural industry, with Scotland being more dependent on this than either the UK as a whole or the EU (Scottish Executive, 2001). In 2016, there were 1.8 million cattle in Scotland (Scottish Government, 2016a). Unlike other parts of the UK, Scotland has a much larger beef sector than dairy sector (McCormick et al., Reference McCormick, Stott, Brülisaue, Vosough Ahmadi and Gunn2010).

Over the past few decades, significant changes have occurred in many farming systems in Scotland, leading in general to systems of specialized production (Scottish Executive, 2001). Technological advances in farming have seen in the growth of large farms. In 2016, 30% of beef cattle (131,000 cows) were in a herd size of 150 animals and over, while 69% of dairy cattle (121,000 cows) were in herds of 150 animals or more (Scottish Government, 2016a).

Scotland's climate can be particularly wet and windy in winter, this, coupled with reduced grazing quality, means that cattle are housed for longer periods of time. The majority of beef cattle and all dairy herds need to be housed for a 6-month or more winter feeding period, which has been a significant constraint on the competitiveness of Scottish farming (House of Commons, Scottish Affairs Committee, 1996). Furthermore, housed cattle are at higher risk of disease such as BRD and BVD. It has been found that in closely confined housing systems, a new born PI animal can infect over 90% of the herd before it has reached 4 months (Houe et al., Reference Houe1993).

BVD in Scotland

In Scotland and the UK as a whole, BVD is considered an endemic disease and the Department for Environment, Food and Rural Affairs (DEFRA) (2006) estimated that BVD costs the cattle sector between £25 and £61 million per year. Furthermore, the economic impact of the disease is most likely underestimated as herd infection is frequently undetected (Brülisauer et al., Reference Brülisauer, Lewis, Ganser, McKendrick and Gunn2010). Studies commissioned by the Scottish Government in 2007 found that, from a bulk milk sample survey of 400 dairy herds, only 22% of the farms studied displayed no evidence of recent BVD exposure, 42% of the farms displayed high antibody titer (indicating recent BVD exposure or vaccination), and 36% of the farms displayed intermediate levels of antibodies. Furthermore, a blood sample study of 300 suckler herds found that 17% of the farms had PI animals (Macrae and Esslemont, Reference Macrae and Esslemont2015).

Since 2009, farmers, vets, and the Scottish Government have been working together on creating and implementing a national BVD eradication program. The introduction of the program, currently entering into phase 5, has seen the level of BVD exposure drop significantly in breeding herds (Scottish Government, 2017). It is believed that BVD eradication will increase the profitability and sustainability of Scotland's cattle business and it has been estimated that BVD eradication from the herd could save the average dairy herd £15,800 per year and the average beef herd £4800 per year (Scottish Government, 2017).

BVD eradication in Scotland

Scotland began its BVD eradication scheme in 2010 with the aim of identifying and removing PI animals from the national herd. Farmers would be encouraged to eliminate BVD from their herds, thereby decreasing the number of PI calves born (Scottish Government, 2017). So far, four phases of the program have been implemented, with phase 5 currently being drafted. Over the past 7 years, the Scottish Government has initiated the legislative obligation for farmers of breeding herds to screen their cattle every year for BVDV and has implemented control measures based on the screening test results. There is also a ban on moving PI animals and suspected PI animals anywhere but directly to slaughter (Scottish Government, 2017).

Phase 1 focused on subsidized screening, with the Scottish Government providing money toward BVD testing for each herd and further funding for veterinary support if the herd tested positive (Scottish Government, 2016b). It was found that 23% of the beef herds tested and 52% of the dairy herds tested had been exposed to BVDV (Scottish Government, 2016b).

Phase 2 of the program, which began at the end of 2011, saw the introduction of mandatory annual BVD screening. There was a requirement for all farmers of breeding cattle herds to test their herds for BVD before a cutoff date, and then on a yearly basis thereafter (Scottish Government, 2016b). In this phase, there were eight testing procedures available; samples of blood, tissue, milk or semen were accepted and could be tested for antibody or for antigen (Scottish Government, 2016b). Bulk milk sampling to establish antibody status was the most common test in dairy herds and antigen blood testing was most often performed to detect PIs, while blood testing was the most common method in beef herds during phase 2 (Duncan et al., Reference Duncan, Gunn and Humphry2016).

The standard check test involves the sampling of five animals per management group (a management group is defined as animals that are housed or grazed together for at least 2 months). All samples must be sent to government-approved laboratories, who then report the results to the Scottish Government and give the herd a status of ‘negative’ or ‘not negative’ (Scottish Government, 2016b). Not-negative herds have evidence of exposure to BVDV, thus more comprehensive testing is needed to identify if there are PI animals in the herd. If a herd has a not-negative status, farmers should screen all new calves born or carry out a whole herd screen as their yearly test. Only cattle that have tested BVDV-negative or those believed to be negative can move from not-negative herds (Scottish Government, 2015).

The third phase came into force at the start of 2014 and was concerned with reducing the spread of infection through three main control measures. Knowingly selling or moving BVDV-infected cattle (both PI and transiently infected animals) was prohibited. Animals identified as BVDV-positive can solely be moved directly to slaughter. Such restrictions are facilitated through the Cattle Tracing System (CTS). A further control measure was the requirement that the BVD status of a herd be declared before selling, thus allowing potential buyers to verify the current BVD status of the herd or animal. The third measure involved a restriction on herds and animals that have not been tested, aimed at farmers who fail to comply with the mandatory testing requirement (Scottish Government, 2016b).

Scotland is currently in stage 4, which began in June 2015 and involves the introduction of enhanced testing and increased movement restrictions. Under stage 4, animals coming from a not negative herd are not permitted to move unless going directly to slaughter or if the individual animal tests negative for BVDV. Replacement animals from untested herds, including imported animals, must now be individually tested.

The number of permitted testing methods has been reduced, with bulk milk tests no longer available. The new measures also include assumed negative status for the mother of a BVDV-negative animal and assumed positive status for the calf of a PI dam (Scottish Government, 2015).

At the end of 2017, the Scottish Government opened public consultations to seek feedback on phase 5 of the eradication scheme (Scottish Government, 2018). The new measures were refined into the following eight proposals:

• • Requirement for cattle keepers to investigate the cause of BVDV exposure in herds that have had a ‘not negative’ status for 13 months or more

• • Restrictions on purchasing or bringing in animals to ‘BVDV-positive’ herds

• • The use of primary or secondary identification tags for tissue tag sampling

• • Requirement to test at least 10% of calves born in a herd in the last 12 months

• • Faster reporting of laboratory results to the national database – from 40 to 5 days

• • Requirement to track PI animals back to their herd of pregnancy risk period and birth (if different)

• • New movement restrictions on animals before their test results have been uploaded to the national database

• • Publishing of the location of ‘BVDV-positive’ herds

Phase 5 is currently being drafted based on these proposals and there is the potential for a sixth phase in the future. Scotland's BVD eradication scheme has been largely successful, with the level of exposure decreasing from 40 to 10% of herds over the past 7 years (Scottish Government, 2017). However, an area of the program that has been less successful has been in overcoming the issue of non-compliant farmers, with some being reluctant to quickly remove PI animals from their herd or not acting to deal with BVDV in their herd (Voas, Reference Voas2017). Furthermore, the final stages of BVD eradication will most likely be the most challenging. As natural immunity diminishes alongside the number of herds exposed, national herds will become ever more susceptible to outbreaks of BVD.

Overview of farming in Spain

In Spain, utilized agricultural area makes up 47% of the whole territory, and when compared with other Western European countries, the proportion of land used for agricultural purposes is low (European Commission, 2010). In total, agriculture constitutes approximately 3.5% of the GDP in Spain, with livestock production making up about 1.2% of the GDP (Castel et al., Reference Castel, Mena, Ruiz and Morales2011). Within the Spanish livestock sector, meat production dominates, accounting for 73%, and milk production is in second place, accounting for 18% of production (Castel et al., Reference Castel, Mena, Ruiz and Morales2011). The area with the highest concentration of cattle, both dairy and sucklers, is the north of Spain (Diéguez et al., Reference Diéguez, Cerviño and Yus2017). Livestock production in Spain has transformed from a domestically oriented to an internationally focused industry, and has moved from an extensive to an intensive industrial model (Ríos-Núñez and Coq-Huelva, Reference Ríos-Núñez and Coq-Huelva2015). This can be seen in terms of the size of agricultural holdings, with a decline in the number of small holdings and an increase in the number of large holdings (European Commission, 2010).

BVD in Spain

The prevalence of BVD in Spain is not clear, due to the fact that few studies have been carried out at national level and the studies that do exist tend to be based on seroprevalence, which at least confirms the circulation of the virus. Such studies report a varied but generally high seroprevalence. For example, 85.7% in Asturias (Mainar-Jaime and Berzal-Herranz, Reference Mainar-Jaime and Berzal-Herranz2001), 91.5% in León (Álvarez et al., Reference Álvarez, González, Álvarez, López and Llamazares1994), 94.2% in Madrid (Vega et al., Reference Vega, Orden, García, Pérez, Ruiz-Santa-Quinteira and De la Fuente2004), 70.9% in Andalucía (Gómez-Pacheco et al., Reference Gómez-Pacheco, Tarradas-Iglesias, Luque-Moreno, Arenas-Casas, Maldonado-Borrego, González and Perea-Remujo2009), and 70.2% in Galicia (Eiras et al., Reference Eiras, Diéguez, Sanjuán, Yus and Arnaiz2009). All of these studies identified BVDV-1 as the circulating strain.

In recent years, the existence of BVDV-2 has been confirmed in isolates in the north of Spain. In Asturias, two adult dairy cows, with no apparent symptoms, were found to be carrying BVDV-2 (strain 2406-2/12) (Aduriz et al., Reference Aduriz, Atxaerandio and Cortabarria2015). In Galicia in 2016, BVDV-2 was found in a 31-month-old animal, and it is believed that this strain was introduced through neighboring farms importing infected animals from other countries (France and Holland) (Factor et al., Reference Factor, Yus, Eiras, Sanjuan, Cerviño, Arnaiz and Diéguez2016). These neighboring farms were found to be lacking in biosecurity measures and did not test incorporations to the herd. Furthermore, over-the-fence contact with neighbor animals was possible.

In 2006, the European Commission funded a study (Lindberg et al., Reference Lindberg, Berriatua, Fourichon, Mintiens and Houe2006a) into how BVD control efforts were performed within EU member states. It found that in Spain, the buying in of PI cattle, including pregnant cows carrying infected fetuses, was believed to be the most significant risk factor (accounting for around 80%) for the introduction of BVDV into previously uninfected herds. The transboundary movement of cattle within Europe is a key area in BVDV transmission, with almost 52,000 PI animals being moved across borders in a year. Countries highly affected in this context were Italy, the Netherlands, and Spain. The second most important risk factor in Spain was from contact with PI animals from other herds at markets, during transportation or at pasture, which was considered to account for approximately 20% of cases of introduction of BVDV into previously uninfected herds.

A number of countries in the EU, including Spain, do not monitor or report on BVD prevalence at the national level. Such countries are more likely to lack a systematic eradication program (Lindberg et al., Reference Lindberg, Berriatua, Fourichon, Mintiens and Houe2006a), as is the case with Spain. BVD eradication in Spain is limited to mainly herd-to-herd control and occasional regional control efforts such as the eradication project being carried out in Galicia (Lindberg et al., Reference Lindberg, Brownlie, Gunn, Houe, Moennig, Saatkamp, Sandvik and Valle2006b).

BVD control in Galicia

The first region of Spain to implement a voluntary program of BVD control was Galicia, which started in 2004 (Diéguez et al., Reference Diéguez, Yus, Sanjuán, Vilar and Arnaiz2008). In the first stage, the initial BVD status of each herd is evaluated in order to differentiate herds with BVDV from those which are BVDV-free. The second stage is the identification and removal of PI animals from herds. Then continual monitoring of herds is performed to ensure the virus is not (re)introduced (Eiras and Arnaiz, Reference Eiras and Arnaiz2010).

Initial sampling and analysis involves serological testing to determine exposure to BVDV in cattle over 1 year old. These samples are analyzed with a commercial enzyme-linked immunosorbent assay test, which detects antibodies against a virus protein. The same test is used in herd monitoring through biannual bulk milk testing and serum testing of heifers over 9 months old (Factor et al., Reference Factor, Yus, Eiras, Sanjuan, Cerviño, Arnaiz and Diéguez2016). In cases where herds show continued high antibody titers, indicating the presence of a PI animal, it is then necessary to test animals individually. It was found that, in 2014, the prevalence of PI animals from all those sampled in farms with suspected BVD was 1.5% (Calvo, Reference Calvo2016). A drawback of these diagnostic techniques is that inactivated vaccines can interfere with results, which should be taken into account when interpreting serological results (Makoschey et al., Reference Makoschey, Sonnemans, Bielsa, Franken, Mars, Santos and Álvarez2007).

The voluntary nature of the program puts it at a disadvantage, resulting in limited coverage; only 60% of cows and 40% of herds are participating (Factor et al., Reference Factor, Yus, Eiras, Sanjuan, Cerviño, Arnaiz and Diéguez2016). However, a noteworthy success of the Galician control program is its growth and expansion throughout the region in the past decade. Studies have shown the number of farms engaging with the program continue to increase (Calvo, Reference Calvo2016; Factor et al., Reference Factor, Yus, Eiras, Sanjuan, Cerviño, Arnaiz and Diéguez2016). A further success of this program has been in improved testing of animals being bought in to herds, improved detection of BVDV exposure in these animals, and in reducing the sale of PI animals (Calvo, Reference Calvo2016). Another positive outcome is that the average age at which PI animals are diagnosed has decreased, from 15.3 months in 2007 to 6.2 months in 2014 (Calvo, Reference Calvo2016). These successes demonstrate the impact of systematic control efforts and highlight the need for a national control program in Spain.

Recommendations for further BVD control in Spain

Proven successful BVD control practices can be extrapolated from existing programs, while keeping at the forefront the unique challenges that each country and region faces:

• • The use of clear and distinct phases, beginning with voluntary participation and progressing to mandatory phases

• • The implementation of a national, state subsidized control program, which covers all animals in the national herd

• • Restrictions on the buying and selling of BVD-positive animals and animals not tested at origin, applying to animals from both the internal and the external markets

• • The creation of a public register of the BVD status of holdings.

• • Movement restrictions of cattle from or to farms with unknown BVD status

• • The promotion of strict biosecurity measures

• • The continuing education of producers in the sector

Overview of farming in Argentina

Agricultural land in Argentina is approximately 54% (World Bank, 2017). In 2016, agriculture accounted for 7.6% of the country's gross domestic product (GDP) (World Bank 2016). Argentina has traditionally been well known for its beef production and held a place as one of the world's largest beef exporters (Guevara and Grünwaldt, Reference Guevara, Grünwaldt and Javed2012). The EU has been a major buyer of Argentinean beef, especially of high-quality fresh beef (Souza-Monteiro and Caswell, Reference Souza-Monteiro and Caswell2004). Despite being ranked the third largest exporter of beef in the world in 2005, Argentina fell to 11th place in 2012, with high export taxes being a likely cause of this decrease (World Bank, 2014). In recent years, there has been a sharp decline in cattle stock, which between 2007 and 2010 had decreased by almost 10 million head (Guevara and Grünwaldt, Reference Guevara, Grünwaldt and Javed2012). While Argentina has gradually lost its place in the world export markets, it remains the country with the highest per capita meat consumption worldwide (56.3 kg per capita per year) and has a strong domestic beef market. The vast majority of beef produced in Argentina is sold in the domestic market; during the period 2001–2010, 84% of Argentina's beef production went to the internal market (Guevara and Grünwaldt, Reference Guevara, Grünwaldt and Javed2012).

Traditionally, beef cattle have been bred through natural service and raised on pasture, where bulls, cows, and calves coexist freely with little intervention (Campero et al., Reference Campero, Moore, Odeon, Cipolla and Odriozola2003). However, the sector is evolving and modernizing, incorporating technological advances such as pasture planting, diet management as well as reproductive technologies like artificial insemination (AI) and estrus synchronization. Feedlots have brought a change to the traditional pastoral cattle systems in Argentina and the number of animals from feedlot destined for slaughter has been increasing in the past decade (Guevara and Grünwaldt, Reference Guevara, Grünwaldt and Javed2012). Argentinian feedlot systems recently accounted for approximately 50% of animals slaughtered (Climate and Clean Air Coalition, 2015).

Argentina also has a large dairy sector. In 2012, the dairy sector had 10,453 farms, where 1,690,581 cows were milked, producing a total of 11,600 million liters of milk per year (Suero et al., Reference Suero, Castignani, Teran and Marino2012).

BVD in Argentina

In Argentina, with its extensive livestock industry, BVD is one of the leading causes of infertility, abortion, and perinatal deaths (Muñoz et al., Reference Muñoz, Lager, Mersich, Zabal, Ulloa, Schudel and Weber1996; Odeón et al., Reference Odeón, Risatti, Kaiser, Leunda, Odriozola, Campero and Donis2003). In most herds, seropositive animals are extremely common, with studies demonstrating that up to 70% of cattle are seropositive to BVDV (Rweyemamu et al., Reference Rweyemamu, Fernandez, Espinosa, Schudel, Lager and Mueller1990; Pacheco and Lager, Reference Pacheco and Lager2003). Even in closed herds, where infection from external sources is extremely unlikely, most calves are infected at a young age, many before they reach 6 months (Gogorza et al., Reference Gogorza, Morán, Larghi, Braun and Esteban2006). A number of BVDV strains have been found to circulate in Argentina, BVDV-1a, BVDV-1b, BVDV-1c and BVDV-2a are all present in the Argentine bovine population (Jones et al., Reference Jones, Zandomeni and Weber2001; Jones and Weber, Reference Jones and Weber2004; Pecora et al., Reference Pecora, Malacari, Ridpath, Perez Aguirreburualde, Combessies, Odeón, Romera, Golemba and Wigdorovitz2014). A study by Julià et al. (Reference Julià, Craig, Jiménez, Pinto and Weber2009) found that BVDV-1, and most likely BVDV-2, circulate in sheep and the study found evidence that PI sheep were natural reservoirs, even without cattle participation.

Several outbreaks of fatal mucosal disease caused by BVDV have been reported over the past two decades in Argentina (Odeon et al., Reference Odeón, Risatti, Kaiser, Leunda, Odriozola, Campero and Donis2003; Lunardi et al., Reference Lunardi, Headley, Lisbôa, Amude and Alfieri2008). A severe outbreak occurred in 2009 in a herd in the southwestern part of Buenos Aires Province, during which 22% of yearling males from the herd died and 12% of the herd was subsequently found to be PI (González Altamiranda et al., Reference González Altamiranda, Kaiser, Weber, Leunda, Pecora, Malacari, Morán, Campero and Odeón2012). A study of this outbreak revealed that the most likely source of infection was AI, using semen contaminated with BVDV (González Altamiranda et al., Reference González Altamiranda, Kaiser, Weber, Leunda, Pecora, Malacari, Morán, Campero and Odeón2012). This demonstrates the risks associated with the semen of PI bulls, compounded by the fact that such bulls show normal growth and development and results of semen analysis can be normal. Furthermore, BVDV is able to survive processing and cryopreservation (Kirkland et al., Reference Kirkland, Mackintosh and Moyle1994; Givens and Waldrop, Reference Givens and Waldrop2004). A further problem with using semen from PI bulls is that it produces notably lower fertilization rates (González Altamiranda et al., Reference González Altamiranda, Kaiser, Weber, Leunda, Pecora, Malacari, Morán, Campero and Odeón2012), which adds to the negative impact that BVDV has on the overall reproductive performance of animals.

Due to the complexity of the illness and the lack of studies into the economic impact of BVD in Argentina, it is difficult to quantify economic losses, but as with other countries where BVD is endemic, such losses are likely to be significant. One study estimated the economic losses of BVD-related abortions at approximately $1,496,880,000 (Argentine pesos) or $100,000,000 (US$) (Odeón, Reference Odeón2016).

Current BVD control in Argentina is based on vaccination using inactivated vaccines. Given the severe negative impact that BVDV has been demonstrated to have on the reproductive performance of cattle and the economic output of the sector, there is a strong argument supporting the need for a systematic control program.

Recommendations for BVD control in Argentina

Using the experience from existing BVD eradication programs, such a program in Argentina should be clearly defined and realistic and should include the following four basic strategies:

• • Education and training

• • Diagnostic testing

• • Elimination of PI cattle

• • Biosecurity and management

BVD is not considered a priority in Argentina, while other diseases such as TB and brucellosis continue to be endemic. Given the economic difficulties facing Argentina, a significant issue in implementing a control program may be in the reluctance of government to subsidize it. It is therefore essential that the scale of BVD and its economic impact are brought to the attention of all parties involved in cattle production and health, including government bodies.

To formulate an appropriate control program, it is essential to know the BVD status of herds in the region. This is initially achieved through the serological profiling of herds. It must be borne in mind that such tests may be adversely affected by the presence of colostral antibodies and vaccine antibodies.

The next step is to carry out further antigen tests on all animals in positive herds and after all births, in order to identify and remove PI animals as quickly as possible. While potentially challenging due to the type of extensive farming in Argentina, such tests should be carried out before weaning at the latest, so as not to lose the traceability between cow and calf.

The different routes through which BVDV could potentially infect or re-infect a herd should be evaluated. The types of biosecurity measures which would have the most impact in Argentina may differ from those given high priority in other regions such as Europe. For example, the low population density in Argentina decreases contact between animals in a herd and makes over-the-fence contact with neighboring herds unlikely, therefore decreasing BVDV transmission. Notwithstanding, the following biosecurity measures have an important role to play in BVD control in the region:

• • Antigen and antibody testing of animals prior to selling and the use of quarantine on farms after purchase, with a new test after 4 weeks to prevent the entry of animals with active infection, PI, or cows carrying PI fetuses

• • Particularly important for Argentina, strict protocols for the detection of the virus in the biological material used in AI and the elimination of contaminated materials.

Given the potential difficulties in implementing such a systematic control program in Argentina, the incorporation of a vaccination program may be a practical and cost-effective measure. This would base long-term control on the protection of breeding herds and the prevention of new PI births. A useful strategy would be to also vaccinate calves at weaning, after their negative diagnosis, to minimize the possibility of respiratory symptomatology. Currently in Argentina, only inactivated BVDV vaccines are licensed and most are formulated with strains of BVDV-1a, with only a few containing strains of BVDV-2, which limits their effectiveness (Pecora et al., Reference Pecora, Malacari, Ridpath, Perez Aguirreburualde, Combessies, Odeón, Romera, Golemba and Wigdorovitz2014). Therefore, the research, development, and approval of new vaccines are fundamental, as well as government accountability in making decisions for the implementation of animal health policies.