key: cord-0033424-p4apvrjc
authors: More, Simon; Bøtner, Anette; Butterworth, Andrew; Calistri, Paolo; Depner, Klaus; Edwards, Sandra; Garin‐Bastuji, Bruno; Good, Margaret; Gortázar Schmidt, Christian; Michel, Virginie; Miranda, Miguel Angel; Nielsen, Søren Saxmose; Raj, Mohan; Sihvonen, Liisa; Spoolder, Hans; Stegeman, Jan Arend; Thulke, Hans‐Hermann; Velarde, Antonio; Willeberg, Preben; Winckler, Christoph; Baldinelli, Francesca; Broglia, Alessandro; Dhollander, Sofie; Beltrán‐Beck, Beatriz; Kohnle, Lisa; Bicout, Dominique
title: Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): bovine viral diarrhoea (BVD)
date: 2017-08-04
journal: EFSA J
DOI: 10.2903/j.efsa.2017.4952
sha: 42a3960ffdb83950e83acd5952d070c6a5e86829
doc_id: 33424
cord_uid: p4apvrjc

Bovine viral diarrhoea (BVD) has been assessed according to the criteria of the Animal Health Law (AHL), in particular criteria of Article 7 on disease profile and impacts, Article 5 on the eligibility of BVD to be listed, Article 9 for the categorisation of BVD according to disease prevention and control rules as in Annex IV and Article 8 on the list of animal species related to BVD. The assessment has been performed following a methodology composed of information collection and compilation, expert judgement on each criterion at individual and, if no consensus was reached before, also at collective level. The output is composed of the categorical answer, and for the questions where no consensus was reached, the different supporting views are reported. Details on the methodology used for this assessment are explained in a separate opinion. According to the assessment performed, BVD can be considered eligible to be listed for Union intervention as laid down in Article 5(3) of the AHL. The disease would comply with the criteria as in Sections 4 and 5 of Annex IV of the AHL, for the application of the disease prevention and control rules referred to in points (d) and (e) of Article 9(1). The assessment here performed on compliance with the criteria as in Section 3 of Annex IV referred to in point (c) of Article 9(1) is inconclusive. The animal species to be listed for BVD according to Article 8(3) criteria are mainly species of the families Bovidae, Cervidae and Camelidae as susceptible species and several mammalian species as reservoirs.

Interpretation Background and Terms of Reference as provided by the requestor

The background and Terms of Reference (ToR) as provided by the European Commission for the present document are reported in Section 1.2 of the scientific opinion on the ad hoc methodology followed for the assessment of the disease to be listed and categorised according to the criteria of Article 5, Annex IV according to Article 9, and 8 within the Animal Health Law (AHL) framework (EFSA AHAW Panel, 2017).

Interpretation of the Terms of Reference

The interpretation of the ToR is as in Section 1.2 of the scientific opinion on the ad hoc methodology followed for the assessment of the disease to be listed and categorised according to the criteria of Article 5, Annex IV according to Article 9, and 8 within the AHL framework (EFSA AHAW Panel, 2017) .

The present document reports the results of assessment on bovine viral diarrhoea (BVD) according to the criteria of the AHL articles as follows:

• Article 7: BVD profile and impacts • Article 5: eligibility of BVD to be listed • Article 9: categorisation of BVD according to disease prevention and control rules as in Annex IV • Article 8: list of animal species related to BVD.

The methodology applied in this opinion is described in detail in a dedicated document about the ad hoc method developed for assessing any animal disease for the listing and categorisation of diseases within the AHL framework (EFSA AHAW Panel, 2017).

This section presents the assessment of BVD according to the Article 7 criteria of the AHL and related parameters (see Table 2 of the opinion on methodology (EFSA AHAW Panel, 2017)), based on the information contained in the fact-sheet as drafted by the selected disease scientist (see Section 2.1 of the scientific opinion on the ad hoc methodology) and amended by the AHAW Panel. Bovine viral diarrhoea virus (BVDV) is a member of the Pestivirus genus of the family Flaviviridae.

3.1.1. Article 7(a) Disease Profile 3.1.1.1. Article 7(a)(i) Animal species concerned by the disease

Parameter 1 -Naturally susceptible wildlife species (or family/orders) Evidence for natural susceptibility of wildlife species Ridpath and Neill, 2016) comes mainly from serological surveys. While these have typically demonstrated the presence of antibodies capable of neutralising BVDV, the possibility that they may in some cases indicate exposure to a different, but related, Pestivirus cannot be excluded. Those species from which BVDV has been isolated (or viral antigen/RNA detected), confirming their susceptibility are underlined below; otherwise natural susceptibility is based on serological evidence. Where only serological evidence of infection exists, it is recognised that due to the cross-reactive nature of pestiviral antibodies it is possible that these are due to infection with other pestiviral species and do not provide definitive evidence of susceptibility to BVDV (Ridpath and Neill, 2016) .

African Buffalo (Syncerus caffer) American Bison (Bison bison) (Ridpath and Neill, 2016) Bighorn Sheep (Ovis canadensis) (Ridpath and Neill, 2016 (Ridpath and Neill, 2016) Pampas Deer (Ozotoceros bezoarticus celer) Red Deer (Cervus elephus) (Ridpath and Neill, 2016) Reindeer (Rangifer tarandus) Roe Deer (Capreolus capreolus) (Ridpath and Neill, 2016) Sika Deer (Cervus nippon) White-Tailed Deer (Odocoileus virginianus) (Ridpath and Neill, 2016) Family Giraffidae Giraffe (Giraffa camelopardalis) (Ridpath and Neill, 2016) Family Antilocapridae Pronghorn (Artilocapra americana) (Ridpath and Neill, 2016) Family Camelidae Alpaca (Vicugna pacos) Dromedary (Camelus dromedarius) Guanaco (Lama guanicoe) Llama (Lama glama) Vicuna (Vicugna vicugna)

Wart Hog (Phacochoerus africanus) Wild Boar (Sus scrofa) (Ridpath and Neill, 2016) Family Traguilidae Mousedeer (Tragulus javanicus) (Grondahl et al., 2003) Order Lagomorpha

Evidence of susceptibility of Leporidae (order Lagomorpha) has been published. A study in wild rabbits in Germany found low levels of neutralising antibodies in 40/100 sera (Fr € olich and Streich, 1998) , although attempts at virus isolation were unsuccessful. A survey in the UK reported a weak positive result by enzyme-linked immunosorbent assay (ELISA) (and with high levels of non-specific binding) in 3/260 wild rabbits (Grant et al., 2015) , with the authors concluding BVDV is not established as an endemic infection of rabbits in the regions of the UK where sampling was conducted (Bachofen et al., 2014; Grant et al., 2015) . More recently, 34/94 sera from European hares were found to contain virus neutralisation (VN) antibodies to a ruminant pestiviruses with none testing positive for viral RNA by real time RT-PCR.

Rabbit (Oryctolagus cuniculus) (Fr € olich and Streich, 1998; Grant et al., 2015) European hare (Lepus europaeus) Parameter 2 -Naturally susceptible domestic species (or family/orders) BVDV is predominantly a pathogen of cattle, but interspecies transmission can occur following contact with sheep, goats and pigs. In common with cattle, infection of sheep can result in the birth of viable persistently infected (PI) lambs. In contrast, the birth of PI offspring appears to be a rare result of in utero infection in goats and pigs .

Family Bovidae

Family Suidae (Pigs)

Parameter 3 -Experimentally susceptible wildlife species (or family/orders)

Challenge of New Zealand White rabbits with BVDV by the intravenous (IV) and oronasal (ON) routes, and via contaminated hay resulted in seroconversion in some or all rabbits in each group in the absence of clinically apparent disease (Bachofen et al., 2014) . All whole blood samples collected from each group during serial bleeds were negative by real time RT-PCR, as were oral swabs (providing no evidence for shedding by this route). Tissue samples and buffy coat were collected from rabbits challenged by the IV and ON routes, with some positive results, particularly following IV challenge. Virus isolation was attempted on ileum collected following IV challenge, with positive results.

IV challenge of pregnant rabbits did not result in clinical signs or increased rates of abortion or stillbirth (Grant et al., 2015) . Relatively few offspring (21%) had evidence of infection by real time RT-PCR at the end of the experiment (maximum 10 days of age), with a proportion of these also seropositive by ELISA. Persistence of infection was therefore not demonstrated.

to be susceptible to infection with BVDV (Baker et al., 1954) , although recent work has suggested that mice can be infected when inoculated by oral and intra-nasal challenge (Seong et al., 2015 (Seong et al., , 2016 .

Parameter 5 -Wild reservoir species (or family/orders) Lack of strict host species specificity raises the possibility of reservoir species, but it has been considered that natural infections in species other than cattle and sheep do not represent a disease problem for control programmes in domestic ruminants (Løken and Nyberg, 2013) . Passler et al. (2016) propose four criteria that a potential wildlife reservoir must satisfy: (1) be susceptible to BVDV, (2) shed BVD (particularly through persistently infected animals), (3) maintain BVDV in the population, (4) have sufficient contact with cattle to allow spillback infections to occur. Applying these criteria to white-tailed deer (Odocoileus virginiansis) in the US, where they have been intensively studied in relation to BVDV, they conclude that they represent a low risk as an important reservoir species in most environments. In general, seroprevalence levels are much lower in wildlife than in cattle in endemic situations, suggesting that the former are spillover hosts rather than true reservoir species. Evermann (2006) suggests three proposed population groups for pestiviral infections: cervid, camelid and domestic ruminants, with pestiviruses (which may be distinct from BVDV) circulating within and, under optimum conditions, between these clusters. While this may result in disease, the potential for limited intrahost spread in the new population is suggested to limit the possibility of this leading to an epidemic in the new population.

In Europe, a number of studies have also investigated the seroprevalence of BVDV in deer, typically to examine their epidemiological importance in the context of national eradication programmes. A serosurvey of free-living deer from regions of Denmark with a relatively high prevalence of cattle herds with a persistent BVD infection status prior to its eradication from cattle found a very low prevalence of cervid infection (Nielsen et al., 2000) . The authors concluded that the positive animals were likely to have resulted from transmission from cattle to deer and that transmission among deer or from deer to cattle was highly unlikely and therefore that the possibility of free-living deer being a source of infection for cattle was remote.

A serological survey in Norway between 1993 and 2000 found 12.3% roe deer to be seropositive to BVDV, with the authors concluding that pestivirus is endemic in this species (Lillehaug et al., 2003) . While they noted the possibility of deer to cattle transmission impacting on eradication and surveillance within the Norwegian eradication programme, this has proven unfounded as demonstrated by the successful completion of the eradication programme (Løken and Nyberg, 2013) .

The role of wild ruminants, including red and roe deer, in the epidemiology of BVDV infections in domestic livestock in Switzerland was investigated (Casaubon et al., 2012) . The authors found that despite regular interactions with farmed ruminants, infection in wild ruminants was sporadic with VN antibodies not found in any of 435 roe deer and detected in only 13/476 red deer (2.7%). They concluded that wildlife was an incidental spillover host rather than a reservoir host for BVDV and as such did not represent a threat to the Swiss national BVDV eradication programme in livestock (Presi and Heim, 2010) .

A recent study in Belgium (Tavernier et al., 2015) of wild roe deer found only 1.3% seropositive, despite an expanding population and regular contact with livestock, concluding that they do not play an important role in the epidemiology of infection in domestic animals.

A similar study was conducted in the south of Spain (Paniagua et al., 2016) where wild ruminant populations have also increased substantially, resulting in the frequent sharing of habitats with domestic livestock. It found only 1 of 892 red deer to be seropositive and concluded that the deer were spillover hosts only and did not represent a risk for domestic ruminants. Another study of sympatric alpine populations of livestock and wild ruminants, including deer in north-west Spain generated similar findings (Fern andez-Aguilar et al., 2016). Grant and others (Grant et al., 2015) consider that a wildlife reservoir in the rabbit (Oryctolagus cuniculus) poses a small but non-zero risk of re-infection for BVDV-free cattle herds. While this is unlikely to be of epidemiological relevance for most control scenarios, it may theoretically play a role in the tail end of an eradication campaign.

Detection of VN antibodies to pestiviruses, including BVDV, in European hares (Lepus europaeus) has led to the suggestion that they may be a wildlife reservoir, particularly in relation to the Pyrenean chamois .

Parameter 6 -Domestic reservoir species (or family/orders) Sheep and goats are susceptible to infection with BVDV. While both sheep and goats PI with BVDV have been described, foetal death and non-viability of lambs are common sequelae of transplacental infection in sheep and viable PI kids are considered a rare result of in utero infection in goats, where reproductive failure or gross pathology of infected foetuses are the likely outcome (Løken, 1995; Bitsch et al., 2000; Krametter-Froetscher et al., 2010; Passler and Walz, 2010) .

3.1.1.2. Article 7(a)(ii) The morbidity and mortality rates of the disease in animal populations

Parameter 1 -Prevalence/Incidence A series of investigations aimed at assessing the prevalence of BVDV infection have been performed in Europe, from the late seventies and into the 21st century, and the results of these at both animal- (Table 1 ) and herd-levels ( Table 2 ) have been reviewed within the position paper published by the EU Thematic network on control of bovine viral diarrhoea virus (BVDV) (2001) .

The general picture is that in many European countries without systematic control in place, or before such measures were implemented, the infection has been/is endemic at a high level with 60-80% of the animals being antibody positive and 1-2% being persistently infected. In many countries, surveys indicated that almost all herds had antibody carriers and approximately half of them had PI animals. However, a few countries had quite a different picture with much lower prevalences. This heterogeneity in the presence of BVDV infection in the absence of systematic control was considered likely to be a reflection of the distribution of risk factors for new BVDV infections and for persistence of the infection in the respective countries.

Where a systematic approach has been adopted in MS, significant progress has been made. The Scandinavian Member States (MS) Sweden, Finland, Denmark have completed eradication programmes (as has Norway) (Stahl and Alenius, 2012; Løken and Nyberg, 2013; Foddai et al., 2014; Norstr € om et al., 2014; Finnish Food Safety Authority Evira, 2016) , while national or regional programmes are under way and have reduced the prevalence of PI births in a number of other MS, including Austria, Germany, Ireland, Scotland and Belgium (Rossmanith et al., 2010; Schirrmeier et al., 2012; Clegg et al., 2016; Duncan et al., 2016; Ribbens et al., 2016) and in Switzerland (Presi et al., 2011) . Parameter 2 -Case-morbidity rate (% clinically diseased animals out of infected ones)

The case-morbidity rate for acute (transient) infections varies with a range of factors, including the age of the animal, its immune status and its reproductive state . The majority of acute infections are considered subclinical. However, infection of a BVDV na € ıve animal results in a transient viraemia which can be associated with short-term leukopenia, lymphopenia and/or thrombocytopenia, apoptosis in the thymus, and pyrexia. The resultant immunosuppression, particularly in calves, can allow other infectious agents to become established, or allow the recrudescence of existing infections resulting in enteric or respiratory disease. Infection of na € ıve breeding animals may have a range of negative outcomes depending on the stage of reproduction, including fertilisation failure, early embryonic death, abortion, congenital defects and the birth of PI offspring which may be weak, undersized and ill-thrifty. Acute infection of sexually active bulls results in a reduction in sperm density and motility, plus an increase in sperm abnormalities .

Following the emergence of BVDV II in North America, much higher case morbidity rates (and mortality rates) were reported (Carman et al., 1998) . The within-herd abortion rate was 44% (3-83%). The mortality rate was 53% (3-83%) for animals under 2 years of age and 9% (2-26%) for older animals. A recent study of BVDV type 2c in Germany reported a case-fatality rate of up to 60% and mortality in outbreak farms varied between 2.3% and 29.5% (Gethmann et al., 2015) . 

*: Note that the antibody detection methods vary between countries as do the cut offs when a herd is considered to have antibody carriers or PI animals. Prevalences are therefore just indicative of the level and not directly comparable between countries.

Persistent infections: PI animals have been shown to be significantly smaller than non-PI animals ( Table 3 ). The annual incidence risk of dying or being slaughtered due to unthriftiness was calculated as 0.28 and 0.31 among 34 PI animals in 10 Danish dairy herds (Houe, 1993) . Observational studies on the impact of infection with BVDV on health and production parameters have been reviewed in the EU Thematic network on control of BVDV (2001) and the results are reproduced below (Table 3) . (anywhere) BVDV is not considered zoonotic, although the ability of BVDV to replicate in human cell lines has been reported in some studies and there are limited reports of detection of virus, viral RNA or antigen in human samples (Giangaspero et al., 1997; Walz et al., 2010; Bratcher et al., 2012) .

3.1.1.4. Article 7(a)(iv) The resistance to treatments, including antimicrobial resistance Parameter 1 -Resistant strain to any treatment even at laboratory level Not applicable to viruses.

3.1.1.5. Article 7(a)(v) The persistence of the disease in an animal population or the environment

Parameter 1 -Duration of infectious period in animals

Transiently infected (TI) animals: 0-14 days (Niskanen et al., 2002; Lindberg and Houe, 2005; Nickell et al., 2011; Sarrazin et al., 2014) .

Persistently infected animals: lifelong (Lindberg and Houe, 2005) .

True latency is not described for BVDV.

Persistent infected animals may be apparently normal and healthy or small, weak and ill-thrifty: they are lifelong carriers and shedders of BVDV (Lindberg and Houe, 2005; .

Parameter 4 -Length of survival (dpi) of the agent and/or detection of DNA in selected matrices (soil, water, air) from the environment (scenarios: high and low T)

In general, pestiviruses including BVDV have limited ability to maintain their infectivity outside the host; it rapidly loses infectivity after contact with organic solvents and pH outside the range of 6.7-9.3, with sensitivity to low pH increasing with environmental temperatures from 4 to 37°C (Stevens, 2009) . The same author also examined the ability of BVDV to survive over a 96-h period on/in a range of surfaces and liquids, with or without mucus, including paper, latex gloves, cotton T-shirt, denim jeans, untreated pine wood, rubber boot, galvanised and enamelled buckets, mineral and salt blocks, total mixed ration (TMR), pen floor soil/manure, water and phosphate buffered saline (PBS).

The probability of virus being present decreased with time, with survival enhanced by the presence of mucus. Modelling predicted no virus present at 96 h in all cases. Virus survival was most prolonged in water and PBS, followed by on latex and enamelled metal, paper, galvanised metal, soil and pine and TMR. No virus was recovered from the cotton T shirt, denim, mineral or salt licks (Stevens, 2009) .

Slurry: 105.2 TCID 50 /50 lL of BVDV was fully inactivated after 3 weeks, 3 days, 3 h, 50 min, 20 min, 5 min and 5 mins at temperatures of 5, 20, 35, 40, 45, 50 and 55°C, respectively (Bøtner and Belsham, 2012) .

Whole milk: BVDV was inactivated when whole milk was heated at 85-92.2°C for 10 min (although viral RNA could still be detected in some samples) (Marley et al., 2009) .

Whole and ground meat: BVDV was consistently inactivated when cooked to ≥ 75°C (Bratcher et al., 2012) .

BVDV is resistant to dry heat, not being significantly inactivated by one hour's exposure to temperatures between 75 and 95°C (Sauerbrei and Wutzler, 2009 ).

3.1.1.6. Article 7(a)(vi) The routes and speed of transmission of the disease between animals, and, when relevant, between animals and humans

Parameter 1 -Types of routes of transmission from animal to animal (horizontal, vertical)

Horizontal: Direct (nose to nose) and airborne over short distances in buildings where persistently infected animals are present and indirect via contaminated equipment, facilities and personnel (Gunn, 1993) . Spread of BVDV by ambient air or other vehicles involving TI animals has never been demonstrated and is most to be of marginal significance (Lindberg and Houe, 2005) . Virus may be shed in the semen of bulls (Rikula et al., 2008) , but avoidance of transmission by this route during artificial insemination using semen collected in MSs can be achieved through compliance with the requirements for intracommunity trade laid down in Council Directive 2003/43/EC 1 or the OIE guidelines on collection and processing of bovine, small ruminant and porcine semen (OIE, 2016b) . BVDV can also be transmitted by embryo transfer, but preliminary evidence indicates that the risk is negligible if in vivo embryos are collected and processed according to OIE guidelines (OIE, 2016a). Adventitious transmission by contaminated live vaccines has also been described (Løken, 1995) . Virus has been recovered from biting and non-biting flies following exposure to PI animals in experimental studies, but with one exception onward transmission of the virus has not been demonstrated (Gunn, 1993; Rikula et al., 2008; OIE, 2016b) .

Vertical: Transient infection of a na € ıve dam during the first third of pregnancy (up to approximately 125 days of gestation) will result in the birth of a PI calf if the foetus is carried to term. All calves born to PI dams will also be PI.

Parameter 2 -Types of routes of transmission between animals and humans (direct, indirect, including food-borne) Not relevant.

Parameter 3 -Incidence between animals and, when relevant, between animals and humans See below.

Parameter 4 -Transmission rate (beta) (from R 0 and infectious period) between animals and, when relevant, between animals and humans A basic reproduction ratio (R 0 ) of 0.25 (95% CI 0.01; 1.95) and 0.24 (95% CI 0.01; 2.11) was estimated for TI animals infected with a virulent BVDV-1b and a virulent BVDV-2a field isolate from Belgium, respectively. After introduction of a PI animal, an R 0 of +∞ (95% CI 1.88; +∞) was calculated. These results support the suggestion that TI animals, compared to PI animals, contribute only a limited amount to BVDV spread (Sarrazin et al., 2014) . Parameter 2 -Type of epidemiological occurrence (sporadic, epidemic, endemic) at MS level

The disease is considered endemic in all MS in the absence of systematic eradication programmes (Tables 1 and 2) .

Where a systematic approach has been adopted in MS, significant progress has been made. The Scandinavian countries Sweden, Finland and Denmark have completed eradication programmes (as has Norway) (Stahl and Alenius, 2012; Løken and Nyberg, 2013; Foddai et al., 2014; Norstr € om et al., 2014; Finnish Food Safety Authority Evira, 2016) , while national or regional programmes are under way and have reduced the prevalence of PI births in a number of other MSs, including Austria, Germany, Ireland, Austria, Scotland and Belgium (Rossmanith et al., 2010; Schirrmeier et al., 2012; Clegg et al., 2016; Duncan et al., 2016; Ribbens et al., 2016) and in Switzerland (Presi et al., 2011) .

Infection is already present in MS.

3.1.1.8. Article 7(a)(viii) The existence of diagnostic and disease control tools

Parameter 1 -Existence of diagnostic tools A range of reliable diagnostic tools for detection of virus, viral antigens, RNA and antibodies are available (see Section 3.1.4.1. Parameter 1).

Parameter 2 -Existence of control tools Three central elements of systematic approaches to control and eradication of BVDV have been identified (Lindberg et al., 2006) : a) biosecurity and possible use of vaccination (Lindberg et al., 2006) aimed at preventing re-introduction of the infection in free herds b) elimination of PI animals from infected herds c) surveillance to monitor the progress of interventions and to rapidly detect new infections.

These have been applied independently, in a number of European countries, with Scandinavia now considered free of infection. Compulsory independent national or regional programmes are currently underway in a number of other countries, including Austria, Belgium, Ireland, Northern Ireland, Germany, Scotland and Switzerland (Stahl and Alenius, 2012; Sarrazin et al., 2013) . These programmes are not compulsory on an EU level.

However, EU level measures are in place to prevent trading of bovine semen and embryos from BVDV-infected donor animals. Council Directive 2003/43/EC lays down the animal health requirements applicable to intra-Community trade and imports of semen of domestic animals of the bovine species. The loss of production due to the disease Parameter 2 -Proportion of production losses (%) by epidemic/endemic situation Health and production losses from observational studies are summarised in Table 3 . Losses attributable to BVD arise from three main sources-reproductive losses, immunosuppression in calves and persistently infected animals (Gunn et al., 2004) . Estimates of economic/financial losses due to BVDV associated with initial outbreaks, the average losses at herd level and at national livestock level have been reviewed in the Report on the EU Thematic Network on control of BVDV. Various studies were carried out on the average financial losses for cattle herds. The estimations range from €30 to €60 per average cow present. At the level of the national livestock sector, studies indicated a loss due to BVDV under endemic conditions of € 15-20 per cow present. Compared to other production diseases such as mastitis and lameness, the financial-economic importance of BVDV can be considered as 'moderate'.

Some results are summarised in Tables 5, 6 and 7 for some countries (EU Thematic network on control of bovine viral diarrhoea virus (BVDV), 2001). The variation in the economic impact of BVDV at dairy farm level in a number of MS arising from uncontrolled output following introduction to a BVDV-naıve herd within year 1 of a 10-year epidemic represented 22%, 7%, 8%, 5%, 8% and 20% of the BVDV-free annuity for the UK, Northern Portugal, Holland, Norway, Italy and Germany, respectively (Gunn et al., 2005) .

Total loss attributable to infection with BVDV in New Zealand dairy herds was estimated at NZ$87 per cow/year in affected herds, and NZ$44.5 million per year overall, based on an estimated 14.6% affected herds (Heuer et al., 2007) .

The maximum annual output losses per cow in 50-cow suckler (cow-calf) beef herds in Scotland where the herd was either initially BVDV-free or of unknown status were estimated at £38.71 and £28.22, respectively (Stott et al., 2012) .

The average annuity equivalent of unchecked losses due to BVDV infection and re-infection in typical British hill suckler (cow-calf) enterprises over a 10-year disease ranged from almost £0/cow to approximately £40/cow per year, depending on the initial disease status of the herd, the initial source of virus, the probability and source of further infection, the probability of virus transmission within the herd and herd size (Gunn et al., 2004) .

Based on data for 1993, the annual financial loss due to BVD in Norway in the absence of control was estimated at approximately NOK 32.5 million (Valle et al., 2005) .

The annual losses to the Irish cattle industry due to BVDV were estimated at €102 million (Stott et al., 2012) (cattle population estimate in 2016: 6,613,400; Central Statistic Office Ireland).

Using an economic welfare model, the net discounted economic gain for Scotland of eradicating BVD from the Scottish dairy herd was estimated at £47 million over a 10-year eradication period (Weldegebriel et al., 2009) .

The annual cost of BVDV in the Australian cattle population was estimated to be AUS $57.9 million . Clinical signs may vary from inapparent to death, depending on a variety of factors including whether the animal is acutely or persistently infected.

Acute (transient) infections: Transient infection of na € ıve female breeding animals may have a range of negative outcomes depending on the stage of reproduction, including fertilisation failure, early embryonic death, abortion, congenital defects and the birth of PI offspring which may be weak, undersized and ill-thrifty; infection of na € ıve bulls may result in decreased sperm motility and density and increase levels of sperm abnormalities . Other clinical signs associated with acute infection include pyrexia, diarrhoea, decreased milk yield, sudden death and haemorrhagic syndrome (Ridpath et al., 2013; Gethmann et al., 2015) .

However, the majority of acute infections are considered subclinical, with seroconversion and recovery occurring 2-3 weeks post-infection (Ridpath et al., 2013; . Even in the absence of clinical signs infection of a BVDV, na € ıve animal results in a transient viraemia which can be associated with short-term leukopenia, lymphopenia and/or thrombocytopenia, apoptosis in the thymus, and pyrexia. The resultant immunosuppression, particularly in calves, can allow other infectious agents to become established, or allow the recrudescence of existing infections resulting in enteric or respiratory disease which may be fatal. Recent work demonstrating a significant reduction in thymic size following challenge of calves with both low and high virulence BVDV strains, accompanied (Ridpath et al., 2013) . Following the emergence of BVDV II in North America, much higher case morbidity rates (and mortality rates) associated with primary infection were reported (Carman et al., 1998) . The within-herd abortion rate was 44% (3-83%). The mortality rate was 53% (3-83%) for animals under 2 years of age and 9% (2-26%) for older animals. A recent study of BVDV type 2c in Germany reported a case-fatality rate of up to 60% while mortality in outbreak farms varied between 2.3% and 29.5% (Gethmann et al., 2015) . Persistent infections: PI animals can be clinically healthy, but some may appear small, weak and ill-thrifty, showing decreased weight gain, stunted growth and chronic ill thrift. PI animals are considered more susceptible to secondary infections leading to poor survivability of most PI animals. The annual incidence risk of dying or being slaughtered due to unthriftiness was calculated as 0.28 and 0.31 among 34 PI animals in 10 Danish dairy herds (Houe, 1993) .

In addition, PI animals are uniquely to susceptible to developing mucosal disease, which is inevitably fatal , with death occurring a few days to a few weeks following its onset.

Parameter 1 -Endangered wild species affected: listed species as in CITES and/or IUCN list

The CITES list contains a number of species in the Families Antilocapridae, Bovidae, Cervidae, Camelidae and Suidae, within the Order Artiodactyla. However, there is no specific data confirming their susceptibility to infection with BVDV (although a related pestivirus has been isolated from pronghorn (Ridpath and Neill, 2016) .

Despite abundant evidence that pestiviruses currently circulate in wildlife populations, the full impact of exposure and prevalence of these infections are largely unknown (Ridpath and Neill, 2016) .

Parameter 3 -Capacity of the pathogen to persist in the environment and cause mortality in wildlife BVDV does not survive for extended periods in the environment (see Section 3.1.1.5 Parameter 4). Despite abundant evidence that pestiviruses currently circulate in wildlife populations, the full impact of exposure and prevalence of these infections are largely unknown (Ridpath and Neill, 2016) .

Parameter (2015), with these being further categorised according to the purpose of the test (Table 8) . Within Europe, availability of laboratories offering tests for both agent identification and detection of the immune response is high, with these commonly accredited to ISO 17025. Kits are readily available commercially.

Parameter 2 -Se and Sp of diagnostic test See Table 9 . It is important that all assays are appropriately validated before use, particularly in relation to their ability or otherwise to detect both BVDV 1 and 2 (and other related pestiviruses) (Bauermann et al., 2012) . 

Parameter 3 -Type of sample matrix to be tested (blood, tissue, etc.) See Table 9 .

Parameter 1 -Types of vaccines available on the market (live, inactivated, DIVA, etc.)

Both live and dead (inactivated vaccines are available (see below).

Parameter 2 -Availability/production capacity (per year)

A search of the websites of the European Medicines Agency (http://www.ema.europa.eu/ema) and the Health Products Regulatory Authority (http://www.hpra.ie/homepage/veterinary) on 15.10.16 provided details of three vaccines currently licensed for use in one or more MSs with datasheet claims relating to fetal protection (Table 10) . No DIVA vaccines are currently licensed. All vaccines licensed in MSs with a claim relating to fetal protection must satisfy the requirements of the BVD Monograph of the European Pharmacopoeia. • Considered the gold standard test, but time-consuming and expensive to perform BVD vaccines are widely available in Europe and worldwide, but specific data on production capacities are lacking.

Parameter 3 -Field protection as reduced morbidity (as reduced susceptibility to infection and/or to disease) All vaccines licensed in MSs with a claim relating to foetal protection must satisfy the requirements of the BVD Monograph of the European Pharmacopoeia.

The role of vaccines in systematic control is as an additional biosecurity measure. In areas where the risk of introducing BVDV infection is known or perceived to be high, one option is to implement systematic vaccination in the initial stages of control/eradication programmes, after removal of PI animals. The need for including a vaccination regime will differ between countries/regions and it will also change over time, as the prevalence of infected herds decreases (EU Thematic network on control of bovine viral diarrhoea virus (BVDV), 2001). Even in this context, there are a number of additional factors that require consideration before using vaccines, including antigenic variation between vaccine and field strains, incorrect use of vaccines, lack of common understanding of the purpose of vaccination, the desirability of 100% efficacy of foetal protection, importance of complying with wider programme elements (not just vaccination), diagnostic confounding and the potential for live BVDV vaccines to be contaminated with adventitious viruses (Lindberg et al., 2006) . There is little information available on the field efficacy of vaccines. A meta-analysis of the efficacy of BVDV vaccination to prevent reproductive disease measured by risk of foetal infection, abortion risk and pregnancy risk revealed significant decreases of nearly 45% in abortions and nearly 85% in foetal infection rate in vaccinated cattle compared with unvaccinated cohorts (Newcomer et al., 2015) . When data relating to field challenge only were included, abortion risk was significantly reduced by 33%, while insufficient data were available for analysis regarding the risk of foetal infection. Additionally, pregnancy risk was increased by approximately 5% in field trials of BVDV vaccinates. It should be noted although that many of the vaccines used in this study are not licensed for use in the EU.

Parameter 4 -Duration of protection See Table 10 .

Parameter 5 -Way of administration See Table 10 . • Prevent introduction of PI animals and carriers OR • Prevent dams in early pregnancy from having direct or indirect contact with sources of BVD virus to avoid creation of PI calves. Lindberg and Alenius (1999) have reviewed risk factors for the introduction of BVDV into non-infected herds, evaluated the perceived need for control for each of these and proposed relevant control measures (Table 11) . At least one susceptible animal in early pregnancy becomes infected due to usage of live vaccine contaminated with noncytopathic BVDV strains in the production process, or disease emerge as a result of recombinations between vaccines and field strains Ridpath and Bolin (1995) and Desport et al. (1996) 

Parameter 2 -Effectiveness of biosecurity measures in preventing the pathogen introduction

Overall, the effectiveness of available biosecurity measures in preventing the entry of BVDV by direct or indirect routes is considered high when applied appropriately. One exception relates to the introduction of pregnant non-PI females carrying PI calves (referred to as Trojan animals) .

Parameter 3 -Feasibility of biosecurity measure

The biosecurity measures described are considered feasible. This has been proven by the number of successfully applied eradication programmes.

Parameter 1 -Available movement restriction measures

The key restriction measure relates to the movement of PI animals. This is readily available through prior testing. Identification of Trojan dams by diagnostic testing prior to movement is not available, but has been addressed in eradication programmes by applying restrictions at herd level for a period following removal of PI animals (EU Thematic network on control of bovine viral diarrhoea virus (BVDV), 2001). Movement of TI animals is considered a much lower risk but is more difficult to address. A range of reliable diagnostic tools for detection of virus, viral antigens, RNA and antibodies are available (see Section 3.1.4.1. Parameter 1).

Additionally, measures are in place to prevent trading of bovine semen and embryos from BVDV-infected donor animals. Council Directive 2003/43/EC lays down the animal health requirements applicable to intra-Community trade and imports of semen of domestic animals of the bovine species.

Parameter 2 -Effectiveness of restriction of animal movement in preventing the between farm spread Prevention of movement of PI animals is considered key to control. The effectiveness of movement controls is clearly dependent on the level of uptake/industry engagement, being most effective in the context of systematic control and least effective when participation/involvement is voluntary (Lindberg et al., 2006) .

Parameter 3 -Feasibility of restriction of animal movement PI animals comprise a small percentage of the population (Houe, 1999) and therefore restricting their movement is feasible. Restricting movements of pregnant females from herds where BVDV has been identified until sufficient time has elapsed to minimise the possibility of the sale of pregnant animals carrying PI calves is also feasible, but is more disruptive to trade and will affect a larger proportion of animals. Measures to prevent movement of TI animals are likely to have a greater impact still, although the duration of the measure at herd level is likely to be much shorter.

Parameter 1 -Available methods for killing animals PI animals are not excluded from the food chain subject to passing appropriate ante-and post-mortem inspection. Therefore, slaughter is normally carried out in abattoirs. Where juvenile PI animals are being culled, there are typically one or a small number of animals per herd which can be slaughtered by veterinary practitioners or knackery operators.

Parameter 2 -Effectiveness of killing animals (at farm level or within the farm) for reducing/stopping spread of the disease Identification and removal of PI animals is recognised to be key to stopping the spread of infection, both within and between farms.

Parameter 3 -Feasibility of killing animals Disposal of small numbers of PI animals either through abattoirs or on farm is feasible (and already happening in eradication programmes).

Availability Parameter 1 -Available disposal option Depending on the age and health of the animal, carcasses and by-products may be disposed of through the abattoir system or by rendering.

Parameter 2 -Effectiveness of disposal option Currently available disposal options are considered effective.

Parameter 3 -Feasibility of disposal option Disposal via abattoir or rendering is already routine.

3.1.5. Article 7(e) The impact of disease prevention and control measures 3.1.5.1. Article 7(e)(i) The direct and indirect costs for the affected sectors and the economy as a whole

Parameter 1 -Cost of control (e.g. treatment/vaccine, biosecurity)

Epidemiological-economic models used to develop a number of decision support tools in several countries at both herd and sectoral/national levels have been reviewed previously (EU Thematic network on control of bovine viral diarrhoea virus (BVDV), 2001). Overall the results at both levels were contradictory, with all studies having in common an emphasis on reducing the risk of re-introduction of BVDV as this had negative consequences on the financial-economic feasibility of prevention and control.

A recent systematic review of economic evaluations of worldwide BVDV control activities found that most studies provided only qualitative values of control activities and did not include an economic methodology in their study design (Richter et al., 2016) .

A loss-expenditure frontier method was used to compare control strategies in Scottish suckler (cow-calf) beef herds to identify strategies with the maximum net benefit from combining output losses and control expenditure (Stott and Gunn, 2008) . Consistent with a previous report (Houe, 2003) , there was no single strategy that generated the best outcome; while the mean net benefit was consistently positive, it varied with herd size and initial herd status (na € ıve or unknown).

A study of producer and consumer benefits arising from eradication of BVDV from Scottish dairy herds estimated that while there was an overall discounted economic gain of £47 million over 10 years, this was unevenly distributed, with milk consumers gaining £11 million and producers with infected herds gaining £39 million, while those with uninfected herds lost £2 million (Stott et al., 2010) .

Parameter 2 -Cost of eradication (culling, compensation) In contrast to other diseases, eradication of BVDV, be it from individual farms or complete livestock sectors, is possible. In other words, the potential gross benefits of eradication of BVDV might be larger than those of other diseases. The costs of such programmes can apparently vary quite a lot, thereby affecting their benefit/cost ratio (BCR). The Norwegian study shows positive financial-economic effects (i.e. a BCR larger than 1) already over a 10-year period, when the annual BVD programme costs were subtracted from the benefits, a net positive value for the entire period of NOK 130 million (Valle et al., 2005) . In contrast, in a French study where it took approximately 15 years to reach breakeven. It should be noted that these two examples applies clearly different control schemes. However, no single advice applicable for all situations exist. Specific conditions could determine the profitability of nation-wide programs (EU Thematic network on control of bovine viral diarrhoea virus (BVDV), 2001).

Analyses of Scandinavian programmes have shown a positive cost benefit. For example Houe (Houe, 2003) reports costs associated with the first 3 years of the Danish eradication programme of approximately $9 million/year, with annual costs of approximately $3.5 million for the following 4 years, with this total of some $41 million cost over 7 years set against annual losses estimated at $20 million prior to eradication.

More recent studies have also proposed a positive cost-benefit to control of BVDV in dairy herds. In New Zealand, the annual cost of BVDV infection to the dairy industry was estimated to be in excess of NZ $23 million per annum, while a range of control options gave rates of return over a 10-year term as high as 123% (Reichel et al., 2008) .

In the Netherlands, the average annual net costs associated with bovine viral diarrhoea were estimated at €27.8 million for the dairy industry, with the most favourable control option examined yielding a positive cost-benefit of 1.5 over a 10-year period (Santman-Berends et al., 2015) .

A study in Ireland predicted the costs of a national eradication programme in Ireland to be €55 million over a 6-year period, generating a positive cost benefit against the estimated annual losses due to BVDV of €102 million (Stott et al., 2012) .

Surveillance and monitoring costs have not been reported by MSs that have completed eradication but are typically based on targeted serological screening of herds using samples including bulk tank milk samples and blood samples collected at abattoirs (Foddai et al., 2014; Norstr € om et al., 2014) . Surveillance and monitoring costs should therefore be lower than eradication costs. The control and eradication programmes that have either been completed or are currently underway in a number of Member States (Stahl and Alenius, 2012) have had good societal acceptance. Control measures which result in the identification and removal of PI animals are anticipated to have a strongly beneficial impact on the welfare of domestic animals by preventing transient infections in this population. The vaccines currently used in the EU are not expected to have side effects such as fetopathy, induction of mucosal disease and immunosuppression impacting on welfare that have been attributed to MLVs used elsewhere (Kelling, 2004; Ridpath, 2013; Griebel, 2015) .

Parameter 2 -Wildlife depopulation as control measure Depopulation of wildlife has not been implemented as a control measure for BVDV.

Parameter 1 -Use and potential residuals of biocides or medical drugs in environmental compartments (soil, water, feed, manure) Biocides and medicinal drugs are not used for control of BVDV.

Control measures are not anticipated to result in mortality in wild species.

This section presents the results of the expert judgement on the criteria of Article 5 of the AHL about BVD (Table 12 ). The expert judgement was based on Individual and Collective Behavioural Aggregation (ICBA) approach described in detail in the opinion on the methodology (EFSA AHAW Panel, 2017). Experts have been provided with information of the disease fact-sheet mapped into Article 5 criteria (see supporting information, Annex A), based on that the experts indicate their Y/N or 'na' judgement on each criterion of Article 5, and the reasoning supporting their judgement.

The minimum number of judges in the judgement was 13. The expert judgement was conducted as described in the methodological opinion (EFSA AHAW Panel, 2017) . For details on the interpretation of the questions, see Appendix B of the methodological opinion (EFSA AHAW Panel, 2017).

As from the legal text of the AHL, a disease is considered eligible to be listed as laid down in Article 5 if it fulfils all criteria of the first set from A(i) to A(v) and at least one of the second set of criteria from B(i) to B(v). According to the assessment methodology (EFSA AHAW Panel, 2017), a criterion is considered fulfilled when the outcome is 'Yes'. According to the results shown in Table 12 , BVD complies with all criteria of the first set and with two criteria of the second set, therefore it is considered eligible to be listed as laid down in Article 5 of the AHL.

This section presents the results of the expert judgement on the criteria of Annex IV referring to categories as in Article 9 of the AHL about bovine viral diarrhoea (Tables 13, 14, 15, 16 and 17) . The expert judgement was based on ICBA approach described in detail in the opinion on the methodology. Experts have been provided with information of the disease fact-sheet mapped into Article 9 criteria (see supporting information, Annex A), based on that the experts indicate their Y/N or 'na' judgement on each criterion of Article 9, and the reasoning supporting their judgement. The minimum number of judges in the judgement was 13. The expert judgement was conducted as described in the methodological opinion (EFSA AHAW Panel, 2017) . For details on the interpretation of the questions, see Appendix B of the methodological opinion (EFSA AHAW Panel, 2017). The disease may result in high morbidity and significant mortality rates NC At least one criterion to be met by the disease:

In addition to the criteria set out above at points 1-2.4, the disease needs to fulfil at least one of the following criteria 3

The disease has a zoonotic potential with significant consequences on public health, including epidemic or pandemic potential OR possible significant threats to food safety N 4(CI) The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals Y 4(PI) The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals Y 5(a)(CI) The disease has a significant impact on society, with in particular an impact on labour markets N 5(a)(PI) The disease has a significant impact on society, with in particular an impact on labour markets N 5(b)(CI) The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals NC 5(b)(PI) The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals NC 5(c)(CI) The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it N 5(c)(PI) The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it N 5(d)(CI) The disease has a significant impact on a long-term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long-term damage to those species or breeds N 5(d)(PI) The disease has a significant impact on a long-term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long-term damage to those species or breeds N Colour code: green = consensus (Yes/No); yellow = no consensus (NC). The disease may result in high morbidity with in general low mortality NC At least one criterion to be met by the disease:

In addition to the criteria set out above at points 1-2.4, the disease needs to fulfil at least one of the following criteria 3

The disease has a zoonotic potential with significant consequences on public health, including epidemic potential OR possible significant threats to food safety N 4(CI) The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals Y 4(PI) The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals Y 5(a)(CI) The disease has a significant impact on society, with in particular an impact on labour markets N 5(a)(PI) The disease has a significant impact on society, with in particular an impact on labour markets N 5(b)(CI) The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals NC 5(b)(PI) The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals NC 5(c)(CI) The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it N 5(c)(PI) The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it N 5(d)(CI) The disease has a significant impact on a long-term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long-term damage to those species or breeds N 5(d)(PI) The disease has a significant impact on a long-term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long-term damage to those species or breeds N Colour code: green = consensus (Yes/No); yellow = no consensus (NC). The disease usually does not result in high morbidity and has negligible or no mortality AND often the most observed effect of the disease is production loss NC AHL assessment on bovine viral diarrhoea (BVD)

www.efsa.europa.eu/efsajournal

This section displays the assessment related to each criterion of Annex IV referring to the categories of Article 9 of the AHL where no consensus was achieved in form of tables (Tables 18, 19 , 20 and 21). The proportion of Y, N or`na 0 answers are reported, followed by the list of different supporting views for each answer.

At least one criterion to be met by the disease: In addition to the criteria set out above at points 1-2.4, the disease needs to fulfil at least one of the following criteria 3

The disease has a zoonotic potential with significant consequences on public health, or possible significant threats to food safety N 4(CI) The disease has a significant impact on the economy of parts of the Union, mainly related to its direct impact on certain types of animal production systems N 4(PI) The disease has a significant impact on the economy of parts of the Union, mainly related to its direct impact on certain types of animal production systems N 5(a)(CI) The disease has a significant impact on society, with in particular an impact on labour markets N 5(a)(PI) The disease has a significant impact on society, with in particular an impact on labour markets N 5(b)(CI) The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals NC 5(b)(PI) The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals NC 5(c)(CI) The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it N 5(c)(PI) The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it N 5(d)(CI) The disease has a significant impact on a long-term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long-term damage to those species or breeds N 5(d)(PI) The disease has a significant impact on a long-term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long-term damage to those species or breeds N Colour code: green = consensus (Yes/No); yellow = no consensus (NC). • PI animals infect a large proportion of susceptible bovines which they come in contact with, thus in herds with PI being present, a very high percentage of the herd will be infected.

Supporting Yes for 2.1 (cat.B,C):

• Transmission rate varies depending on the type of infected animal (for PI animals is high for TI is lower) and on the contact structure on the farm.

Reasoning supporting the judgement Supporting Yes for 2.4 (cat.A):

• The disease may result in high morbidity as high numbers of animals may be infected when PI animals are present. Mortality can be significant due to high case-fatality in PI animals.

Supporting Yes for 2.4 (cat.B):

• Most animals are infected with acute infection and then cured. Only PI animals eventually die.

• High number of animals may be TI by a PI.

Supporting Yes for 2.4 (cat.C):

• In endemic situations, there may be some mortality in PI animals, but production losses are the most observed effect. • Currently, the disease is limited to MSs without voluntary control programmes (and those at the start of a programme). Primarily, it is a welfare concern (particularly in calves) in sequelae associated with transient infection. There is evidence for an abortion rate of 44%.

• Secondary infections can have an impact on animal welfare.

Supporting No:

• Most animals are subclinically infected, thus there is no welfare concern. If there really was, trade without any controls would not be freely allowed and eradication would be compulsory rather than voluntary.

Supporting na:

• There is only data about the American situation and no evidence indicating that large numbers of animals could be affected in Europe.

Reasoning supporting the judgement Supporting Yes:

• BVD would impact all MSs if current controls were relaxed. There would be welfare implications for all animals that present with clinical signs.

• If BVDV is introduced to a na € ıve population, there are abortions, stillbirths and weak calves with persistent infection. This affects welfare in the affected farms.

Supporting No:

• Currently, there are no EU wide controls on BVD. Some MSs are BVD-free and recognised as such by the EU, others are operating independent control/eradication programmes designed specifically for their own situations and these may be submitted to the EU for recognition. There are a number of licensed BVD vaccines available and even without vaccination most animals are subclinically infected, thus there is, as such, no welfare concern impacting large numbers of animals. The disease has existed and currently exists apparently without such animal welfare impacts on large numbers of animals and trade has been freely allowed without any controls, unless disease freedom or a control programme has been recognised by the EU for individual MSs, without any issue.

3.3.2. Outcome of the assessment of criteria in Annex IV for bovine viral diarrhoea for the purpose of categorisation as in Article 9 of the AHL As from the legal text of the AHL, a disease is considered fitting in a certain category (A, B, C, D or E corresponding to point (a) to point (e) of Article 9(1) of the AHL) if it is eligible to be listed for Union intervention as laid down in Article 5(3) and fulfils all criteria of the first set from 1 to 2.4 and at least one of the second set of criteria from 3 to 5(d) as shown in Tables 13-17. According to the assessment methodology (EFSA AHAW Panel, 2017), a criterion is considered fulfilled when the outcome is 'Yes'. With respect to different type of impact where the assessment is divided into current and potential impact, a criterion will be considered fulfilled if at least one of the two outcomes is 'Y' and, in case of no 'Y', the assessment is inconclusive if at least one outcome is 'NC'.

A description of the outcome of the assessment of criteria in Annex IV for BVD for the purpose of categorisation as in Article 9 of the AHL is presented in Table 22 . According to the assessment here performed, BVD complies with the following criteria of the Sections 1 to 5 of Annex IV of the AHL for the application of the disease prevention and control rules referred to in points (a) to (e) of Article 9(1): 1) To be assigned to category A, a disease needs to comply with all criteria of the first set (1, 2.1-2.4) and according to the assessment BVD complies with criterion 2.3, but not with 1 and 2.2 and this assessment is inconclusive on compliance with criteria 2.1 and 2.4. To be eligible for category A, a disease needs to comply additionally with one of the criteria of the second set (3, 4, 5a-d) and BVD complies with criterion 4, but not with criteria 3, 5a, 5c and 5d and this assessment is inconclusive on compliance with criterion 5b. 2) To be assigned to category B, a disease needs to comply with all criteria of the first set (1, 2.1-2.4) and according to the assessment BVD complies with criteria 1 and 2.3, but not with 2.2 and this assessment is inconclusive on compliance with criteria 2.1 and 2.4. To be eligible for category B, a disease needs to comply additionally with one of the criteria of the second set (3, 4, 5a-d) and BVD complies with criterion 4, but not with criteria 3, 5a, 5c and 5d and this assessment is inconclusive on compliance with criterion 5b. 3) To be assigned to category C, a disease needs to comply with all criteria of the first set (1, 2.1-2.4) and according to the assessment BVD complies with criteria 1, 2.2 and 2.3 and this assessment is inconclusive on compliance with criteria 2.1 and 2.4. To be eligible for category C, a disease needs to comply additionally with one of the criteria of the second set (3, 4, 5a-d) and BVD does not comply with criteria 3, 4, 5a, 5c and 5d and this assessment is inconclusive on compliance with criterion 5b. 4) To be assigned to category D, a disease needs to comply with criteria of Sections 1, 2, 3 or 5 of Annex IV of the AHL and with the specific criterion D of Section 4, with which BVD complies. 5) To be assigned to category E, a disease needs to comply with criteria of Sections 1, 2 or 3 of Annex IV of the AHL and/or the surveillance of the disease is necessary for reasons relating to animal health, animal welfare, human health, the economy, society or the environment. The latter is applicable if a disease fulfils the criteria as in Article 5, with which BVD complies.

This section presents the results of the assessment on the criteria of Article 8(3) of the AHL about BVD. The Article 8(3) criteria are about animal species to be listed, as it reads below: 

AHL assessment on bovine viral diarrhoea (BVD)

www.efsa.europa.eu/efsajournal • According to the assessment here performed, bovine viral diarrhoea meets the criteria as in Sections 4 and 5 of Annex IV of the AHL, for the application of the disease prevention and control rules referred to in points (d) and (e) of Article 9(1) of the AHL. According to the assessment here performed, it is inconclusive whether bovine viral diarrhoea complies with the criteria as in Section 3 of Annex IV of the AHL, for the application of the disease prevention and control rules referred to in point (c) of Article 9(1) of the AHL. Compliance of bovine viral diarrhoea with the criteria as in Section 3 is dependent on a decision on criteria 2.1, 2.4 and 5(b).

TOR 2b: for each of the diseases which was found eligible to be listed for Union intervention, a list of animal species that should be considered candidates for listing in accordance with Article 8 of the AHL.

• According to the assessment here performed, the animal species that can be considered to be listed for bovine viral diarrhoea according to Article 8(3) of the AHL are, as reported in Table 23 in Section 3.4 of the present document, several species of the families Bovidae, Cervidae and Camelidae, giraffe, pronghorn, mouse-deer, pig, rabbit, European hare, and some mouse species as susceptible species; cattle, sheep, rabbit and European hare can be considered to be listed as reservoir species.

Experimental infection of rabbits with bovine viral diarrhoea virus by a natural route of exposure

Virus diarrhea in cattle

Antigenic relationships between Bovine viral diarrhea virus 1 and 2 and HoBi virus: Possible impacts on diagnosis and control

Control of bovine viral diarrhea virus infection without vaccines. The Veterinary clinics of North America

Experiences from the Danish programme for eradication of bovine virus diarrhoea (BVD) 1994-1998 with special reference to legislation and causes of infection

Virus survival in slurry: analysis of the stability of foot-and-mouth disease, classical swine fever, bovine viral diarrhoea and swine influenza viruses

Inactivation at various temperatures of bovine viral diarrhea virus in beef derived from persistently infected cattle

Epidemiologic studies of the occurrence of bovine virus diarrhea/mucosal disease in 2892 cattle in 95 dairy farms

Epidemiology of bovine virus diarrhoea in cattle on communal alpine pastures in Switzerland

Severe acute bovine viral diarrhea in Ontario

Bovine viral diarrhea virus in free-ranging wild ruminants in Switzerland: low prevalence of infection despite regular interactions with domestic livestock

Temporal trends in the retention of BVD+ calves and associated animal and herd-level risk factors during the compulsory eradication programme in Ireland

The European hare (Lepus europaeus) as a potential wild reservoir for ruminant pestiviruses

Comparison of ear notch immunohistochemistry, ear notch antigen-capture ELISA, and buffy coat virus isolation for detection of calves persistently infected with bovine viral diarrhea virus

Bovine viral diarrhoea virus seroprevalence and vaccination usage in dairy and beef herds in the Republic of Ireland

Viral recombination in noncytopathogenic bovine viral diarrhoea virus genomes in the lymph nodes of persistently infected animals

Difficulties arising from the variety of testing schemes used for bovine viral diarrhoea virus (BVDV)

Prevalence of bovine virus diarrhoea virus viraemia

Scientific opinion on an ad hoc method for the assessment on listing and categorisation of animal diseases within the framework of the Animal Health Law

Pestiviral infection of llamas and alpacas

Animal diseases in Finland

Quantitative assessment of the risk of introduction of bovine viral diarrhea virus in Danish dairy herds

Challenges for bovine viral diarrhoea virus antibody detection in bulk milk by antibody enzyme-linked immunosorbent assays due to changes in milk production levels

Pr € avalenz und klinische Symptomatik persistenter BVD-virusinfektionen in Rinderbest € anden Niedersachsens

Serologic evidence of bovine viral diarrhea virus in free-ranging rabbits from Germany

Transient elimination of circulating bovine viral diarrhoea virus by colostral antibodies in persistently infected calves: a pitfall for BVDV-eradication programs? Veterinary Microbiology

BVD-2 outbreak leads to high losses in cattle farms in Western Germany

Genotypic analysis of the 5'-untranslated region of a pestivirus strain isolated from human leucocytes

Testing of bulk tank milk from Northern Ireland dairy herds for viral RNA and antibody to bovine viral diarrhoea virus

Assessment of the rabbit as a wildlife reservoir of bovine viral diarrhea virus: serological analysis and generation of trans-placentally infected offspring

BVDV vaccination in North America: risks versus benefits

Bovine viral diarrhoea (BVD) infections-control and eradication programme in breeding herds in Slovenia

Characterisation of a pestivirus isolated from persistently infected mousedeer (Tragulus javanicus)

Role of fomites and flies in the transmission of bovine viral diarrhoea virus

Modelling and costing BVD outbreaks in beef herds

Assessing economic and social pressure for the control of bovine viral diarrhoea virus

Serological studies of mucosal disease virus in England and Wales

Economic effects of exposure to bovine viral diarrhea virus on dairy herds in New Zealand

Comparison of five diagnostic methods for detecting bovine viral diarrhea virus infection in calves

Survivorship of animals persistently infected with bovine virus diarrhoea virus (BVDV)

Epidemiology of bovine viral diarrhea virus. The Veterinary clinics of North America

Epidemiological features and economical importance of bovine virus diarrhoea virus (BVDV) infections

Economic impact of BVDV infection in dairies

Prevalence of bovine virus diarrhoea (BVD) in 19 Danish dairy herds and estimation of incidence of infection in early pregnancy

Prevalence of bovine virus diarrhoea virus viraemia in cattle in the UK

Evolution of bovine viral diarrhea virus vaccines. The Veterinary clinics of North America

Pestivirus infection in sheep and goats in West Austria

A simple, rapid and reliable enzyme-linked immunosorbent assay for the detection of bovine virus diarrhoea virus (BVDV) specific antibodies in cattle serum, plasma and bulk milk

Bovine viral diarrhoea virus ('pestivirus') in Australia: to control or not to control?

Bovine viral diarrhoea: pathogenesis and diagnosis

Natural infection with bovine virus diarrhoea virus in a dairy herd: a spectrum of symptoms including early reproductive failure and retained placenta

Frequency of appearance of persistent BVD virus infections and their effects on the cattle population

Antibodies to ruminant alpha-herpesviruses and pestiviruses in Norwegian cervids

Principles for eradication of bovine viral diarrhoea virus (BVDV) infections in cattle populations

Effect of bovine viral diarrhoea virus infection on average annual milk yield and average bulk milk somatic cell counts in Swedish Dairy Herds

Characteristics in the epidemiology of bovine viral diarrhea virus (BVDV) of relevance to control

The control of bovine viral diarrhoea virus in Europe: today and in the future

Serological study on Bovine Viral diarrhoea virus infection in pig population in poland between

Ruminant pestivirus infections in animals other than cattle and sheep. The Veterinary clinics of North America

Pestivirus infections in Norway. Serological investigations in cattle, sheep and pigs

Epidemiological pattern and risk factors associated with bovine viral-diarrhoea virus (BVDV) infection in a non-vaccinated dairy-cattle population from the Asturias region of Spain

Bovine viral diarrhea virus is inactivated when whole milk from persistently infected cows is heated to prepare semen extender

Health status of bulls used for natural breeding on farms in south west Scotland

Prevalence and epidemiological features of bovine viral diarrhoea virus infection in Lithuania

Clinical consequences of a bovine virus diarrhoea virus infection in a dairy herd: a longitudinal study

Pestivirus infections in ruminants other than cattle

Efficacy of bovine viral diarrhea virus vaccination to prevent reproductive disease: a meta-analysis

Onset and duration of transient infections among antibody-diverse beef calves exposed to a bovine viral diarrhea virus persistently infected calf

Bovine virus diarrhea virus in free-living deer from Denmark

Determination of level of antibodies to bovine virus diarrhoea virus (BVDV) in bulk tank milk as a tool in the diagnosis and prophylaxis of BVDV infections in dairy herds

Effects of infection with bovine virus diarrhoea virus on health and reproductive performance in 2 13 dairy herds in one county in Sweden

Primarily BVDV-infected calves as transmitters of the infection

Failure to spread bovine virus diarrhoea virus infection from primarily infected calves despite concurrent infection with bovine coronavirus

Prevalence and geographic distribution of bovine viral diarrhoea (BVD) infection in Finland

Bovine Viral Diarrhoea

Collection and processing of in vivo derived embryos from livestock and equids

Collection and processing of bovine, small ruminant and porcine semen

Absence of circulation of Pestivirus between wild and domestic ruminants in southern Spain

Bovine viral diarrhea virus infections in heterologous species

Bovine viral diarrhea virus (BVDV) in white-tailed deer (Odocoileus virginianus)

Identification of herd-specific bovine viral diarrhoea virus isolates from infected cattle and sheep

Prevalence of antibodies to bovine virus diarrhoea virus and other viruses in bulk tank milk in England and Wales

Prevalence of bovine viral diarrhea virus infection in bulls in artificial insemination centers in Poland

BVD eradication in Switzerland-a new approach

Bovine viral diarrhea (BVD) eradication in Switzerland-experiences of the first two years

Does control of bovine viral diarrhoea infection make economic sense?

Results of the first year of the mandatory BVDV control program in Northern-Belgium

Economic evaluation of bovine viral diarrhoea virus control activities worldwide: a systematic review

Delayed onset postvaccinal mucosal disease as a result of genetic recombination between genotype 1 and genotype 2 BVDV

Challenges in identifying and determining the impacts of infection with pestiviruses on the herd health of free ranging cervid populations

Comparison of acute infection of calves exposed to a high-virulence or low-virulence bovine viral diarrhea virus or a HoBi-like virus

Transmission of bovine viral diarrhoea virus through the semen of acutely infected bulls under field conditions

Large scale assessment of the effect associated with bovine viral diarrhoea virus infection on fertility of dairy cows in 6149 dairy herds in

The occurrence of BVD virus infections in lower Austrian dairy farms

The effect of infection with bovine viral diarrhea virus on the fertility of Swiss dairy cattle

Evaluation of the epidemiological and economic consequences of control scenarios for bovine viral diarrhea virus in dairy herds

Serological and virological BVDV prevalence and risk factor analysis for herds to be BVDV seropositive in Belgian cattle herds

Virulence comparison and quantification of horizontal bovine viral diarrhoea virus transmission following experimental infection in calves

Testing thermal resistance of viruses

The first year of obligatory BVD control in Germany -diagnostic strategies, results and experiences

Prevalence of bovine virus diarrhoea virus infection in Belgian white blue cattle in Southern Belgium

Experimental infection of mice with bovine viral diarrhea virus

Experimental infection with cytopathic bovine viral diarrhea virus in mice induces megakaryopoiesis in the spleen and bone marrow

BVDV control and eradication in Europe-an update

Frequency and cost of health problems in Swiss dairy cows and their calves

The persistently infected bovine viral diarrhea virus individual: prevalence, viral survival, and impact within commercial feeding systems

Use of a benefit function to assess the relative investment potential of alternative farm animal disease prevention strategies

Modelling the effects of previous infection and re-infection on the costs of bovine viral diarrhoea outbreaks in beef herds

Predicted costs and benefits of eradicating BVDV from Ireland

Prevalence of bovine viral diarrhoea virus in cattle farms in Hungary

Transmission of bovine virus diarrhoea virus by blood feeding flies

Serologic screening for 13 infectious agents in roe deer (Capreolus capreolus) in Flanders

Ten years of bovine virus diarrhoea virus (BVDV) control in Norway: a cost-benefit analysis

A survey for BVDV antibodies in cattle farms in Slovakia and genetic typing of BVDV isolates from imported animals

Natural changes in the spread of bovine viral diarrhoea virus (BVDV) among Estonian cattle

Persistent bovine pestivirus infection localized in the testes of an immuno-competent, non-viraemic bull

Influence of new infection with bovine virus diarrhoea virus on udder health in Norwegian dairy cows

Results achieved by a national programme for the eradication of bovine virus diarrhoea

ACVIM consensus statement on control of bovine viral diarrhea virus in ruminants

Evaluation of producer and consumer benefits resulting from eradication of bovine viral diarrhoea (BVD) in Scotland, United Kingdom

Detection of the bovine viral diarrhoea virus (BVDV) in young beef cattle in eastern and south-eastern regions of Poland

'3. Animal species or groups of animal species shall be added to this list if they are affected or if they pose a risk for the spread of a specific listed disease because: a) they are susceptible for a specific listed disease or scientific evidence indicates that such susceptibility is likely; or b) they are vector species or reservoirs for that disease, or scientific evidence indicates that such role is likely'.For this reason, the assessment on Article 8 criteria is based on the evidence as extrapolated from the relevant criteria of Article 7, i.e. the ones related to susceptible and reservoir species or routes of transmission, which cover also possible role of biological or mechanical vectors. 2 According to the mapping, as presented in Table 5 , Section 3.2 of the scientific opinion on the ad hoc methodology (EFSA AHAW Panel, 2017), the main animal species to be listed for BVD according to the criteria of Article 8(3) of the AHL are as displayed in Table 23 .

TOR 1: for each of those diseases an assessment, following the criteria laid down in Article 7 of the AHL, on its eligibility of being listed for Union intervention as laid down in Article 5(3) of the AHL;• According to the assessment here performed, bovine viral diarrhoea complies with all criteria of the first set and with two criteria of the second set and therefore can be considered eligible to be listed for Union intervention as laid down in Article 5(3) of the AHL.TOR 2a: for each of the diseases which was found eligible to be listed for Union intervention, an assessment of its compliance with each of the criteria in Annex IV to the AHL for the purpose of categorisation of diseases in accordance with Article 9 of the AHL;