- Email: [email protected]
Efficacy of a voluntary BVDV control programme: Experiences from the Netherlands
The Veterinary Journal 245 (2019) 55–60
Contents lists available at ScienceDirect
The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl
Efficacy of a voluntary BVDV control programme: Experiences from the Netherlands L. van Duijn* , A.M.B. Veldhuis, M.H. Mars, B. de Roo, T.J.G.M. Lam GD Animal Health, 7400 AA Deventer, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 13 December 2018
The outcomes of a voluntary bovine viral diarrhoea virus (BVDV) control programme that has been in place in the Netherlands since 1997 were analysed. This ‘BVDV-free’ programme was studied in dairy herds in the period 1 August 2007 to 1 August 2013. The programme was based on a test and cull approach at the herd level, after which the BVDV status was monitored by testing young stock for antibodies against BVDV or by antigen testing of newborn calves. One of the challenges of the programme was that, without any legislation or subsidies, farmers had to be motivated to pay all costs involved, with eradication of BVDV from their farm as the only incentive. During the study period, the percentage of dairy farms with a ‘BVDV-free’ status in the Netherlands increased from 13% to 24%, while the prevalence of active BVDV infections in Dutch dairy herds decreased. This may be related to the increasing number of participants in the ‘BVDV-free’ programme. © 2018 Elsevier Ltd. All rights reserved.
Keywords: Dairy cattle Bovine viral diarrhoea virus Control programme Eradication
Introduction Bovine viral diarrhoea virus (BVDV) occurs worldwide and is associated with a complex of diseases, varying from subclinical to fatal disease (Walz et al., 2010). Several European countries have national or regional programmes to control or eradicate the virus (Stahl and Alenius, 2012). An important feature of the epidemiology of BVDV is the existence of persistently infected animals (PIs). Due to the continuous shedding of large amounts of virus, PIs are the most important source of the virus and the main reason why herds remain infected (Lindberg and Houe, 2005). Some countries, for example Denmark and Norway, have been successful in eradicating BVDV and have attained a ‘BVDV-free’ status, which is maintained through a monitoring system (Norstrom et al., 2014). These countries follow what is commonly referred to as the ‘Scandinavian approach’, in which an initial herd status is determined by serological screening. Herds with evidence of recent infection are required to undergo whole herd screening in order to identify PIs. Other countries, such as Germany and Ireland (GreiserWilke et al., 2003; Graham et al., 2014), follow the ‘Swiss approach’ (Presi and Heim, 2010; Presi et al., 2011), in which, instead of serological herd screening, PIs are directly identified by individual testing for BVDV antigen. A country’s chosen approach to eradicate BVDV, either voluntary or compulsory, is based on a combination of
* Corresponding author. E-mail address: [email protected] (L. van Duijn). https://doi.org/10.1016/j.tvjl.2018.12.016 1090-0233/© 2018 Elsevier Ltd. All rights reserved.
factors, such as density of the cattle population, BVDV prevalence, technical constraints and political considerations. In The Netherlands, a voluntary programme, designated the ‘BVDV-free’ programme was introduced in 1997 with the aim to control BVDV at the herd level. The programme was based on the identification and removal of PIs, followed by monitoring BVDV status at the herd level. Out of several alternative BVDV programmes available, the ‘BVDV-free’ programme has the most participants. Alternative approaches are the ‘BVDV bulk milk’ programme, based on quarterly bulk milk samples that are tested for antibodies against BVDV, the ‘BVDV young stock antibody monitor’, in which five calves are tested for antibodies against BVDV twice per year, and the ‘BVDV young stock PI check’, in which all calves aged 1-5 months are tested for BVDV antigen three times per year. All of these approaches are less strict than the ‘BVDV-free’ programme and do not result in a ‘BVDV-free’ status. In view of the low number of participating herds in each of these alternative schemes, they will not be discussed further in this paper. At the end of 2017, 49% of all dairy farmers and 7% of beef farmers in the Netherlands participated in the ‘BVDV-free’ programme. The aim of this study was to describe the test results of herds participating in the ‘BVDV-free’ programme in the Netherlands during the period 2007-2013. Objectives were: (1) to estimate whether testing of young stock for BVDV antibodies (the ‘spot test’) is an effective tool for monitoring ‘BVDV-free’ herd status; (2) to estimate the percentage of herds with circulating BVDV among Dutch dairy herds with an unknown BVDV status; and (3) to determine the risk of BVDV circulation in herds with a ‘BVDV-free’ status.
56
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60
Materials and methods The Dutch cattle industry At the end of the study period (2013), in the Netherlands, approximately 4 million head of cattle were kept in 36,000 herds. The majority of cattle (70%) were in dairy herds (19,000). Eight per cent of the non-dairy herds (17,000) were veal calf herds (2000), housing approximately 23% of all cattle. Beef herds and suckling cow herds housed approximately 7% of cattle, with a majority having a herd size <20 animals. Approximately half of all dairy herds were closed herds. Bovine viral diarrhoea virus-free programme The ‘BVDV-free’ programme is based on: (1) the identification and removal of PIs; (2) testing of purchased animals for BVDV; and (3) monitoring of the herds’ ‘BVDV-free’ status by biannual testing of young stock for BVDV antibodies (‘spot test’). Vaccination against BVDV is not part of the ‘BVDV-free’ programme, but is allowed. During the study period, only inactivated vaccines were commercially available in the Netherlands. The intake procedure starts with screening the herd for PIs (Fig. 1). All cattle >1 month of age are tested. Lactating cows are tested by performing a quantitative reverse transcriptase (RT)-PCR on a bulk milk sample and the remaining animals are tested by performing a quantitative RT-PCR on pooled serum samples, followed by an antigen ELISA on individual samples from positive pools (Mars and van Maanen, 2005). In addition, calves that are < 1 month of age at the time of intake and will be reared on the farm, along with calves > 1 month of age born in the 10 months after the first screening, are tested for the presence of BVDV. Antigen ELISAs are performed on ear notch samples collected from newborn calves directly after birth and serum samples collected from calves >1 month of age. PIs are removed from the farm within 8 weeks after the initial test result. BVDV positive animals can be be resampled and tested to determine if they are PIs or transiently infected animals (confirmation testing). The advised interval between both samplings is 3 weeks. If the confirmation test is negative, the animal is not considered a PI and can remain on the farm. If all PIs are removed and no PIs have been detected in the previous 10 months, the herd attains a ‘BVDV-free’ status. The ‘BVDV-free’ status is monitored by testing a convenience sample of five calves at the age of 8–12 months using an ELISA for detection of antibodies against BVDV (‘spot test’) twice a year in order to detect circulation of BVDV (Fig. 1, option 2) (Houe, 1992). Only occasionally less than five calves are sampled, in which cases the data are not included in the analysis. As an alternative to the spot test, all newborn calves that are being reared on the farm can be tested for the presence of BVDV in blood or ear notch samples (Fig. 1, option 1). If the spot test indicates that circulation of BVDV might have occurred, or if a BVDV positive animal is found, the herd loses its ‘BVDV-free’ status. The herd regains its ‘BVDV-free’ status only if further testing shows that there are no PIs in the herd, or if the PI is removed and no PIs are found for another 10 months (Fig. 1). The herd maintains its ‘BVDV-free’ status as long as no more than one antibody positive calf is detected in the spot test.
When 2/5 calves test seropositive, the ‘BVDV-free’ status is lost and an ‘extended spot test’ has to be implemented, in which five new calves are sampled and the two positive calves are resampled. The herd retains its ‘BVDV-free’ status when, in the extended spot test, a maximum of two calves are antibody positive; then, the spot test is repeated 6 months later (‘spot test +6 months’). If greater than or equal to three calves are seropositive, the extended spot test is considered to be positive and a ‘cohort test’ is performed. In such a cohort test, blood samples of all young stock 1–16 months of age are collected and tested for BVDV. If in the cohort testing no BVDV-positive animal is found, the herd retains its ‘BVDVfree’ status. Otherwise, the BVDV positive animals are considered to be PIs and are removed from the farm. Newborn calves raised on the farm are tested for BVDV until no more BVDV positive animals are detected for a 10 month period. Diagnostic testing An in-house PCR (Mars and van Maanen, 2005) was used for detection of BVDV in pooled serum samples (15–20 animals), in combination with an antigen ELISA based on Erns (HerdCheck BVDV Ag serum, IDEXX) applied to individual serum samples from PCR positive pools. In 2012, the conventional PCR was replaced by a quantitative RT-PCR, based on the method described by Gaede et al. (2003), and validated as 100% sensitive and 100% specific relative to the conventional PCR (Mars and van Maanen, 2005). The antigen ELISA was validated for use on serum of calves >4 weeks of age; the sensitivity of the antigen ELISA was estimated to be 99% and the specificity was estimated to be 99.5% relative to PCR (Mars and van Maanen, 2005). A conventional PCR was applied to bulk milk as described by Mars and van Maanen (2005); this PCR was validated for herds with a maximum herd size of 130 milking cows. In 2010, additional data were analysed in 11 herds. Bulk milk samples (one or two samples per herd, depending on the herd size) were tested by PCR in serial dilutions. All cattle in these herds were tested individually for BVDV. On the basis of the number of PIs, the number of adult cattle and the limit of detection, a maximum herd size to be tested with a bulk milk sample could be set to 300 milking cows, a cost effective way of screening (Reichel et al., 2016). In herds with more than 130 lactating cows (before 2010) or more than 300 lactating cows (after 2010), blood samples were collected from individual animals or bulk milk samples were collected at two different intervals, with no more than the maximum allowed number of animals in the bulk milk sample, in such a way that all lactating animals were tested in one of these samples. The p80 blocking ELISA (Priocheck BVDV antibody ELISA, Thermofisher, formerly CEDI Diagnostics) was used for antibody testing in serum and bulk milk. Using this blocking ELISA in a sample of five sentinel calves, a sensitivity of 96% and a specificity of 99.9% for detection of a within-herd prevalence of animals with BVDV antibodies of 70% was estimated (Mars and van Maanen, 2005). Data collection and study period Herd data were obtained from an automated certification administration system at GD Animal Health. All available test results of herds participating in the
Fig. 1. Flow chart of the bovine viral diarrhoea virus (BVDV)-free programme as practised in the Netherlands, with a test and cull phase in blue, a monitoring phase in green via antigen testing of newborn calves (option 1) or a spot test in young stock (option 2) and a removal phase for persistently infected animals (PIs) in red.
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60 ‘BVDV-free’ programme during the period 1 August 2007 to 1 August 2013 were included. To estimate the prevalence of active BVDV infection in dairy herds in The Netherlands, a random sample of dairy farms was selected out of a data set comprising all dairy farms with an unknown BVDV status using the ‘sample’ procedure in Stata/SE software version 14. Subsequently, farmers were invited to participate in a cross-sectional study in 2007 (n = 384), 2009 (n = 291) and 2011 (n = 287). Participating farmers were asked to have their private veterinary practitioner collect blood samples for a spot test. Herds with three or more positive samples were considered to have had recent BVDV circulation. The following descriptive results of the ‘BVDV-free’ programme during 20072013 are presented in this paper on a yearly basis: (1) the frequency distribution of spot test outcomes; (2) the percentage of herds that had two positive samples or a positive spot test (3 positive samples); (3) the spot test outcomes after a preceding favourable (negative) spot test; (4) the percentage of cohorts that had BVDV positive animals distributed per spot test category; (5) the spot test outcomes following favourable cohort testing; and (6) the age distribution of BVDV positive animals in cohort testing. In each of the parameters, censoring of herds, after leaving the programme, was taken into account.
Results Spot test During the study period, 31,975 spot tests were performed; of these spot tests, 98% (from 4857 unique herds) consisted of five blood samples collected from five animals per farm from 8–12 months of age and therefore were complete (Table 1). In 87% of these spot tests, no antibodies were detected, indicating no sign of BVDV circulation within the sampled group. In 8% of spot tests, only one animal was seropositive; this result did not lead to any further follow-up for the herd (Fig. 1). In 625 (2%) of spot tests, two samples tested positive for antibodies. This was considered to be an ambiguous result, so an extended spot test was required; resampling was performed in 482 (77%) of these herds (Fig. 2). The other herds either terminated their participation in the programme or did specific resampling in consultation with GD Animal Health, based on the suspicion of development of antibodies due to previous vaccination. Of these 482 herds, 192 had three or more seropositive calves at resampling and therefore cohort testing was commenced. This cohort testing was performed within 6 months in 141 herds; in 26 of these herds, at least one BVDV positive animal was found. In 4% of spot tests, antibodies were detected in three or more samples, indicative of BVDV circulation in the herd. In each year, an average of 6% of herds participating in the ‘BVDV-free’ programme had a spot test result that led to cohort testing in order to trace PIs on the farm. This percentage declined over time, while the number of herds participating in the ‘BVDV-free’ programme increased (Fig. 3). The number of seropositive animals in the initial spot test and in the spot test performed 6 months later (spot test +6 months) are presented in Table 2. At a spot test +6 months after a previous spot test with no seropositive animals, 3% of farms required cohort testing. At the spot test +6 months after a previous spot test with one seropositive animal, 8% of farms required cohort testing. At the
Table 1 Results of complete bovine viral diarrhoea virus spot tests (antibody testing of five animals aged 8–12 months) of 4857 unique herds collected in the period from 1 August 2007 until 1 August 2013. Number of seropositive calves
Number of spot tests
%
0 1 2 3 4 5 Total
27,115 2385 625 326 287 504 31,242
86.8 7.6 2.0 1.0 0.9 1.6 100
57
spot test +6 months after a previous spot test with two seropositive animals, 9% of farms required cohort testing (Table 2). Cohort testing BVDV positive animals were identified in 49% of herds that performed cohort testing. Cohort testing led to the detection of one or more virus positive animals in 18% of herds with two seropositive animals, 54% of herds with three or more seropositive animals and 68% if all five of the spot test samples were positive for antibodies against BVDV (Table 3). Twenty-eight percent of spot tests with three to five antibody positive samples were not followed by cohort testing within 6 months; reasons for this failure to follow-up included additional sampling because of antibodies due to vaccination or farmers terminating participation in the programme. No PIs were identified in 51% of herds in which cohort testing was performed; however, although no PIs were detected in these herds, more seropositive calves were detected in the spot test +6 months in these herds (Table 4) than in the overall total of all spot tests (Table 1). The more calves that were seropositive in the spot test preceding this negative cohort testing, the more calves were antibody positive in the spot test +6 months. If antibodies were detected in all five animals in the preceding spot test, but no PI was found, antibodies were also detected in five animals in 42% of spot test +6 months, whereas only 26% of spot tests +6 months that were preceded by five seropositive animals had no seropositive animals (Table 4). In 57% of this group, the spot test +6 months had three or more antibody positive animals, indicating virus circulation and therefore leading to repeated cohort testing. Confirmation testing A total of 1122 cohort tests were performed in 911 unique herds; of these, 522 herds had one or more BVDV positive animals. Within these positive cohort tests, 20,213 animals were tested for BVDV, of which 782 were positive. A birth date was available for 757 of these calves; BVDV positive animals were on average 6.8 months of age at the time of detection (Fig. 4). Two animals >20 months of age were BVDV positive; these animals were retested and were found to be transiently infected. Of the 522 herds in which BVDV positive animals were found after cohort testing, 90 (17%) performed confirmation testing; animals were resampled at the correct time point in 51/522 (57%) herds and virus was detected at resampling in 47/51 (92%) herds. At the animal level, 42% of retested animals were PIs; on average, these were 6.6 months old at the time of confirmation. Circulation of bovine viral diarrhoea virus among dairy herds with an unknown status The prevalence of herds with active BVDV infections among dairy herds with an unknown BVDV status was estimated to be 24% (95% confidence interval, CI, 19.5–28.3%), 23% (95% CI 18.3–28.3%) and 16% (95% CI 11.7–20.4%) in 2007, 2009 and 2011, respectively. In the same period the proportion of participants in the ‘BVDV-free’ and other BVDV control programmes increased from 23% to 39% (Fig. 5). Discussion Over a period of 20 years, experience was gained with a voluntary approach to BVDV control in the Netherlands. In the ‘BVDV-free’ programme, PIs were identified and culled, after which the BVDV status was monitored on the basis of the spot test. Data analysis over 6 years (1 August 2007 to 1 August 2013)
58
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60
Intake cattle Testing all Spot testfor virus (lactating animals in bulkmilk)
Intake cattle virus Testing Extenall ded spotfor test (lactating animals in bulkmilk)
Intake cattle for virus Testing allResult (lactating animals in bulkmilk)
Intake 0-2 seropositive animals Testing all cattle for virus (n = 290) (lactating animals in bulkmilk)
Intake Testing all cattlestatus for virus BVDV-free (lactating animals in bulkmilk)
2 seropositive animals in spot test ( n = 625)
3 or more seropositive animals (n = 192)
No BVD-virus (n = 115)
BVDV-free status
BVD-virus (n = 26)
Removal PI + 9 months virus testing
Cohort (n = 141)
Fig. 2. Flow chart of an extended spot test, after a spot test (antibody testing of five animals 8–12 months of age) with two animals being seropositive for antibodies against bovine viral diarrhoea virus (BVDV).
Fig. 3. Number of bovine viral diarrhoea virus (BVDV)-free herds monitored, based on spot testing in the ‘BVDV-free’ programme and the percentage of herds with a positive spot test.
Table 2 Results of bovine viral diarrhoea virus spot test (numbers and percentages of seropositive calves) 6 months after a previous spot test (spot test +6 months), with the preceding spot test having 0, 1 or 2 seropositive calves; spot tests with three or more seropositive animals lead to cohort testing. Preceding spot test
0 1 2
Spot test +6 months
Total
0
1
2
3
4
5
20,532 (90%) 1554 (78%) 286 (70%)
1412 (6%) 225 (11%) 60 (15%)
342 (1%) 72 (4%) 21 (5%)
173 (1%) 35 (2%) 14 (3%)
137 (1%) 38 (2%) 12 (3%)
242 (1%) 75 (4%) 13 (3%)
demonstrated that a voluntary programme can be successful, leading to an increasing number of ‘BVDV-free’ herds and a decrease in re-infection with BVDV in these herds. A single seropositive animal in the spot test may be caused by a false positive test result, vaccination induced antibodies or antibodies passively acquired via colostrum uptake (Fulton et al., 2004). In the Netherlands, vaccination is allowed and was implemented in a limited number of herds during the study period.
22,838 (100%) 1999 (100%) 406 (100%)
Since vaccine-induced antibodies may result in a positive spot test (Makoschey et al., 2007), it is advised to select unvaccinated animals for the spot test. A single seropositive animal in the spot test can also be caused by contact between animals infected with BVDV and the sampled age group, for example if a PI left the farm or died very young and therefore did not have the time to infect more animals in the herd (Houe, 1992). In the current ‘BVDV-free’ programme in the Netherlands, a follow up of a spot test with one
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60
59
Table 3 Percentage of cohorts with one or more bovine viral diarrhoea virus (BVDV) positive animals after two, three, four or five seropositive calves in the spot test. Number of seropositive calves
Number of herds required cohort testing
Number of herds that performed cohort testing <6 months
Percentage cohorts with BVDV positive animal (s)
2 3 4 5
192 326 287 504
141 201 190 416
18.4 29.9 49.5 67.8
Table 4 Distribution of bovine viral diarrhoea virus spot test results (numbers and percentages of seropositive calves) 6 months after a previous spot test (spot test +6 months), following negative cohort testing, as related to the number of positive calves in the preceding spot test. Preceding spot test
Spot test +6 months
2 3 4 5
45 56 30 22
0 (51%) (58%) (56%) (26%)
Total 1
2
19 (22%) 17 (18%) 6 (11%) 8 (10%)
8 4 4 6
3 (9%) (4%) (7%) (7%)
Fig. 4. Frequency distribution of the age of bovine viral diarrhoea virus (BVDV) positive animals in the ‘BVDV-free’ programme in the Netherlands during the period 2007–2013 at time of detection.
seropositive animal is advised, since cohort testing is costly and expenditures should be weighed against the chance of finding a PI. No BVDV positive animals were found in 51% of all cohorts tested. In these cohorts, animals that caused the spot test to be positive, by transmitting BVDV, may have been too young to be tested for BVDV, may have died at a young age (Duffell and Harkness, 1985) or may have left the farm for fattening (14–35 days after birth). Finding no PI does not mean that no BVDV infection occurred, as indicated by the subsequent spot test result, which had a higher than average chance of being positive. Thus, antibody detection indicates virus circulation in the herd, even if PIs are no longer present. Therefore, once a spot test is positive, it might be worthwhile advising farmers to test all newborn animals for BVDV (Fig. 1, option 1) in order to detect PIs as early as possible, instead of continuing with monitoring based on the spot test only. When the preceding spot test revealed two antibody positive animals, 70% of these herds had no seropositive animals in the spot test +6 months. Therefore, an additional sampling step was introduced, on the basis of which only 40% of these herds had to undertake cohort testing; this additional sampling thus prevented 60% of cohort testing (Fig. 2), considered to be economically worthwhile.
6 3 0 3
(7%) (3%) (0%) (4%)
4
5
3 (3%) 9 (9%) 7 (13%) 10 (12%)
7 (8%) 8 (8%) 7 (13%) 35 (42%)
88 97 54 84
(100%) (100%) (100%) (100%)
The detection of PIs at an average of 7 months of age is consistent with the biannual spot test frequency (Fig. 4). As a consequence, BVDV can be present in the herd for a relatively long period of time. A higher spot test frequency might reduce the age of animals in which PIs are found, thus reducing the chance of other animals in the herd becoming infected. Another way to find PIs at a younger age is by performing ear notch testing of newborn calves (Fig. 1, option 1). Single spot tests from randomly selected ‘non-participating’ dairy farms demonstrated that 16–24% of herds had active BVDV infections during the study period (Fig. 5). In the same period, the percentage of ‘BVDV-free’ farms having a positive spot test result was 6% per year on the basis of biannual testing. This shows that ‘BVDV-free’ herds have a lower risk of having BVDV circulation on their farm than farms with an unknown BVDV status. During the study period, the percentage of ‘BVDV-free’ herds with a positive spot test decreased from 7% (95% CI 6.0–8.1%) to 5% (95% CI 4.3– 5.8%) per year. The indication of BVDV circulation on dairy farms with an unknown BVDV status also declined from 24% (95% CI 19.5–28.3%) to 16% (95% CI 11.7–20.4%) during the study period. This decline may be caused by an increase in the proportion of participants in the ‘BVDV-free’ programme (Fig. 5), leading to a decrease in the number of PIs in the national cattle population. It is possible that herds with BVDV problems are more likely to participate in the ‘BVDV-free’ programme, in which case the remaining herds with an unknown BVDV status might be less likely to be BVDV positive. Other reasons for this decrease in prevalence could be further implementation of biosecurity measures (van Schaik et al., 2002) or an increase in the uptake of vaccination. Even though the prevalence of BVDV is declining, it will be difficult to eradicate BVDV from the Netherlands as long as not all farmers participate in a control programme, maintaining the risk of reintroduction (Santman-Berends et al., 2015). Eradication from the entire country would be facilitated by legislative support or industry pressure to introduce quality assurance schemes (Lindberg et al., 2006). Conclusions Analysis of the BVDV control programme in the Netherlands demonstrates that a voluntary programme can be successful, as suggested by an increasing number of ‘BVDV-free’ herds and a decrease in circulation of BVDV in these herds. The spot test, as well
60
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60
Fig. 5. Distribution of dairy herds in different bovine viral diarrhoea virus (BVDV) categories: (1) ‘BVDV-free’ according to the ‘BVDV-free’ programme; (2) participating in any BVDV control programme but considered not to be ‘BVDV-free’; (3) BVDV status unknown by year in the period 2007–2013; and (4) percentage of herds with a positive spot test (antibody testing of five animals aged 8–12 months) in dairy herds with an unknown BVDV status in 2007, 2009 and 2011, with 95% confidence intervals.
as the combination of a spot test and extended spot test, is an efficient and effective tool to monitor the ‘BVDV-free’ status of a herd and to detect PI animals. Since 2007, the proportion of Dutch dairy herds with active BVDV infections has decreased, which may be related to the increasing number of participants in the ‘BVDVfree’ programme. Conflict of interest statement None of the authors has any financial or personal relationships that could inappropriately influence or bias the content of the paper. References Duffell, S.J., Harkness, J.W., 1985. Bovine virus diarrhoea-mucosal disease infection in cattle. Vet. Rec. 117, 240–245. Fulton, R.W., Briggs, R.E., Payton, M.E., Confer, A.W., Saliki, J.T., Ridpath, J.F., Burge, L. J., Duff, G.C., 2004. Maternally derived humoral immunity to bovine viral diarrhea virus (BVDV) 1a, BVDV1b, BVDV2, bovine herpesvirus-1, parainfluenza-3 virus bovine respiratory syncytial virus, Mannheimia haemolytica and Pasteurella multocida in beef calves, antibody decline by halflife studies and effect on response to vaccination. Vaccine 22, 643–649. Gaede, W., Gehrmann, B., Korber, R., 2003. Viramikereliminerung: Effektives herdenscreening durch kombination von RT-PCR und antigen-ELISA in blutund milchproben. Berl. Munch. Tierarztl. Wochenschr. 116, 234–239. Graham, D.A., Lynch, M., Coughlan, S., Doherty, M.L., O’Neill, R., Sammin, D., O’Flaherty, J., 2014. Development and review of the voluntary phase of a national BVD eradication programme in Ireland. Vet. Rec. 174, 67. Greiser-Wilke, I., Grummer, B., Moennig, V., 2003. Bovine viral diarrhoea eradication and control programmes in Europe. Biologicals 31, 113–118.
Houe, H., 1992. Serological analysis of a small herd sample to predict presence or absence of animals persistently infected with bovine viral diarrhoea virus (BVDV) in dairy herds. Res. Vet. Sci. 53, 320–323. Lindberg, A., Brownlie, J., Gunn, G.J., Houe, H., Moennig, V., Saatkamp, H.W., Sandvik, T., Valle, P.S., 2006. The control of bovine viral diarrhoea virus in Europe: today and in the future. Rev. Sci. Tech. 25, 961–979. Lindberg, A., Houe, H., 2005. Characteristics in the epidemiology of bovine viral diarrhea virus (BVDV) of relevance to control. Prev. Vet. Med. 72, 55–73. Makoschey, B., Sonnemans, D., Bielsa, J.M., Franken, P., Mars, M.H., Santos, L., Alvarez, M., 2007. Evaluation of the induction of NS3 specific BVDV antibodies using a commercial inactivated BVDV vaccine in immunization and challenge trials. Vaccine 25, 6140–6145. Mars, M.H., van Maanen, C., 2005. Diagnostic assays applied in BVDV control in The Netherlands. Prev. Vet. Med. 72, 43–48. Norstrom, M., Jonsson, M.E., Akerstedt, J., Whist, A.C., Kristoffersen, A.B., Sviland, S., Hopp, P., Wahlstrom, H., 2014. Estimation of the probability of freedom from bovine virus diarrhoea virus in Norway using scenario tree modelling. Prev. Vet. Med. 116, 37–46. Presi, P., Heim, D., 2010. BVD eradication in Switzerland — a new approach. Vet. Microbiol. 142, 137–142. Presi, P., Struchen, R., Knight-Jones, T., Scholl, S., Heim, D., 2011. Bovine viral diarrhea (BVD) eradication in Switzerland — experiences of the first two years. Prev. Vet. Med. 99, 112–121. Reichel, M.P., Lanyon, S.R., Hill, F.I., 2016. Moving past serology: diagnostic options without serum. Vet. J. 215, 76–81. Santman-Berends, I.M., Mars, M.H., van Duijn, L., van Schaik, G., 2015. Evaluation of the epidemiological and economic consequences of control scenarios for bovine viral diarrhea virus in dairy herds. J. Dairy Sci. 98, 7699–7716. Stahl, K., Alenius, S., 2012. BVDV control and eradication in Europe — an update. Jpn. J. Vet. Res. 60 (Suppl), S31–S39. van Schaik, G., Schukken, Y.H., Nielen, M., Dijkhuizen, A.A., Barkema, H.W., Benedictus, G., 2002. Probability of and risk factors for introduction of infectious diseases into Dutch SPF dairy farms: a cohort study. Prev. Vet. Med. 54, 279–289. Walz, P.H., Grooms, D.L., Passler, T., Ridpath, J.F., Tremblay, R., Step, D.L., Callan, R.J., Givens, M.D., 2010. Control of bovine viral diarrhea virus in ruminants. J. Vet. Intern. Med. 24, 476–486.
Contents lists available at ScienceDirect
The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl
Efficacy of a voluntary BVDV control programme: Experiences from the Netherlands L. van Duijn* , A.M.B. Veldhuis, M.H. Mars, B. de Roo, T.J.G.M. Lam GD Animal Health, 7400 AA Deventer, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 13 December 2018
The outcomes of a voluntary bovine viral diarrhoea virus (BVDV) control programme that has been in place in the Netherlands since 1997 were analysed. This ‘BVDV-free’ programme was studied in dairy herds in the period 1 August 2007 to 1 August 2013. The programme was based on a test and cull approach at the herd level, after which the BVDV status was monitored by testing young stock for antibodies against BVDV or by antigen testing of newborn calves. One of the challenges of the programme was that, without any legislation or subsidies, farmers had to be motivated to pay all costs involved, with eradication of BVDV from their farm as the only incentive. During the study period, the percentage of dairy farms with a ‘BVDV-free’ status in the Netherlands increased from 13% to 24%, while the prevalence of active BVDV infections in Dutch dairy herds decreased. This may be related to the increasing number of participants in the ‘BVDV-free’ programme. © 2018 Elsevier Ltd. All rights reserved.
Keywords: Dairy cattle Bovine viral diarrhoea virus Control programme Eradication
Introduction Bovine viral diarrhoea virus (BVDV) occurs worldwide and is associated with a complex of diseases, varying from subclinical to fatal disease (Walz et al., 2010). Several European countries have national or regional programmes to control or eradicate the virus (Stahl and Alenius, 2012). An important feature of the epidemiology of BVDV is the existence of persistently infected animals (PIs). Due to the continuous shedding of large amounts of virus, PIs are the most important source of the virus and the main reason why herds remain infected (Lindberg and Houe, 2005). Some countries, for example Denmark and Norway, have been successful in eradicating BVDV and have attained a ‘BVDV-free’ status, which is maintained through a monitoring system (Norstrom et al., 2014). These countries follow what is commonly referred to as the ‘Scandinavian approach’, in which an initial herd status is determined by serological screening. Herds with evidence of recent infection are required to undergo whole herd screening in order to identify PIs. Other countries, such as Germany and Ireland (GreiserWilke et al., 2003; Graham et al., 2014), follow the ‘Swiss approach’ (Presi and Heim, 2010; Presi et al., 2011), in which, instead of serological herd screening, PIs are directly identified by individual testing for BVDV antigen. A country’s chosen approach to eradicate BVDV, either voluntary or compulsory, is based on a combination of
* Corresponding author. E-mail address: [email protected] (L. van Duijn). https://doi.org/10.1016/j.tvjl.2018.12.016 1090-0233/© 2018 Elsevier Ltd. All rights reserved.
factors, such as density of the cattle population, BVDV prevalence, technical constraints and political considerations. In The Netherlands, a voluntary programme, designated the ‘BVDV-free’ programme was introduced in 1997 with the aim to control BVDV at the herd level. The programme was based on the identification and removal of PIs, followed by monitoring BVDV status at the herd level. Out of several alternative BVDV programmes available, the ‘BVDV-free’ programme has the most participants. Alternative approaches are the ‘BVDV bulk milk’ programme, based on quarterly bulk milk samples that are tested for antibodies against BVDV, the ‘BVDV young stock antibody monitor’, in which five calves are tested for antibodies against BVDV twice per year, and the ‘BVDV young stock PI check’, in which all calves aged 1-5 months are tested for BVDV antigen three times per year. All of these approaches are less strict than the ‘BVDV-free’ programme and do not result in a ‘BVDV-free’ status. In view of the low number of participating herds in each of these alternative schemes, they will not be discussed further in this paper. At the end of 2017, 49% of all dairy farmers and 7% of beef farmers in the Netherlands participated in the ‘BVDV-free’ programme. The aim of this study was to describe the test results of herds participating in the ‘BVDV-free’ programme in the Netherlands during the period 2007-2013. Objectives were: (1) to estimate whether testing of young stock for BVDV antibodies (the ‘spot test’) is an effective tool for monitoring ‘BVDV-free’ herd status; (2) to estimate the percentage of herds with circulating BVDV among Dutch dairy herds with an unknown BVDV status; and (3) to determine the risk of BVDV circulation in herds with a ‘BVDV-free’ status.
56
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60
Materials and methods The Dutch cattle industry At the end of the study period (2013), in the Netherlands, approximately 4 million head of cattle were kept in 36,000 herds. The majority of cattle (70%) were in dairy herds (19,000). Eight per cent of the non-dairy herds (17,000) were veal calf herds (2000), housing approximately 23% of all cattle. Beef herds and suckling cow herds housed approximately 7% of cattle, with a majority having a herd size <20 animals. Approximately half of all dairy herds were closed herds. Bovine viral diarrhoea virus-free programme The ‘BVDV-free’ programme is based on: (1) the identification and removal of PIs; (2) testing of purchased animals for BVDV; and (3) monitoring of the herds’ ‘BVDV-free’ status by biannual testing of young stock for BVDV antibodies (‘spot test’). Vaccination against BVDV is not part of the ‘BVDV-free’ programme, but is allowed. During the study period, only inactivated vaccines were commercially available in the Netherlands. The intake procedure starts with screening the herd for PIs (Fig. 1). All cattle >1 month of age are tested. Lactating cows are tested by performing a quantitative reverse transcriptase (RT)-PCR on a bulk milk sample and the remaining animals are tested by performing a quantitative RT-PCR on pooled serum samples, followed by an antigen ELISA on individual samples from positive pools (Mars and van Maanen, 2005). In addition, calves that are < 1 month of age at the time of intake and will be reared on the farm, along with calves > 1 month of age born in the 10 months after the first screening, are tested for the presence of BVDV. Antigen ELISAs are performed on ear notch samples collected from newborn calves directly after birth and serum samples collected from calves >1 month of age. PIs are removed from the farm within 8 weeks after the initial test result. BVDV positive animals can be be resampled and tested to determine if they are PIs or transiently infected animals (confirmation testing). The advised interval between both samplings is 3 weeks. If the confirmation test is negative, the animal is not considered a PI and can remain on the farm. If all PIs are removed and no PIs have been detected in the previous 10 months, the herd attains a ‘BVDV-free’ status. The ‘BVDV-free’ status is monitored by testing a convenience sample of five calves at the age of 8–12 months using an ELISA for detection of antibodies against BVDV (‘spot test’) twice a year in order to detect circulation of BVDV (Fig. 1, option 2) (Houe, 1992). Only occasionally less than five calves are sampled, in which cases the data are not included in the analysis. As an alternative to the spot test, all newborn calves that are being reared on the farm can be tested for the presence of BVDV in blood or ear notch samples (Fig. 1, option 1). If the spot test indicates that circulation of BVDV might have occurred, or if a BVDV positive animal is found, the herd loses its ‘BVDV-free’ status. The herd regains its ‘BVDV-free’ status only if further testing shows that there are no PIs in the herd, or if the PI is removed and no PIs are found for another 10 months (Fig. 1). The herd maintains its ‘BVDV-free’ status as long as no more than one antibody positive calf is detected in the spot test.
When 2/5 calves test seropositive, the ‘BVDV-free’ status is lost and an ‘extended spot test’ has to be implemented, in which five new calves are sampled and the two positive calves are resampled. The herd retains its ‘BVDV-free’ status when, in the extended spot test, a maximum of two calves are antibody positive; then, the spot test is repeated 6 months later (‘spot test +6 months’). If greater than or equal to three calves are seropositive, the extended spot test is considered to be positive and a ‘cohort test’ is performed. In such a cohort test, blood samples of all young stock 1–16 months of age are collected and tested for BVDV. If in the cohort testing no BVDV-positive animal is found, the herd retains its ‘BVDVfree’ status. Otherwise, the BVDV positive animals are considered to be PIs and are removed from the farm. Newborn calves raised on the farm are tested for BVDV until no more BVDV positive animals are detected for a 10 month period. Diagnostic testing An in-house PCR (Mars and van Maanen, 2005) was used for detection of BVDV in pooled serum samples (15–20 animals), in combination with an antigen ELISA based on Erns (HerdCheck BVDV Ag serum, IDEXX) applied to individual serum samples from PCR positive pools. In 2012, the conventional PCR was replaced by a quantitative RT-PCR, based on the method described by Gaede et al. (2003), and validated as 100% sensitive and 100% specific relative to the conventional PCR (Mars and van Maanen, 2005). The antigen ELISA was validated for use on serum of calves >4 weeks of age; the sensitivity of the antigen ELISA was estimated to be 99% and the specificity was estimated to be 99.5% relative to PCR (Mars and van Maanen, 2005). A conventional PCR was applied to bulk milk as described by Mars and van Maanen (2005); this PCR was validated for herds with a maximum herd size of 130 milking cows. In 2010, additional data were analysed in 11 herds. Bulk milk samples (one or two samples per herd, depending on the herd size) were tested by PCR in serial dilutions. All cattle in these herds were tested individually for BVDV. On the basis of the number of PIs, the number of adult cattle and the limit of detection, a maximum herd size to be tested with a bulk milk sample could be set to 300 milking cows, a cost effective way of screening (Reichel et al., 2016). In herds with more than 130 lactating cows (before 2010) or more than 300 lactating cows (after 2010), blood samples were collected from individual animals or bulk milk samples were collected at two different intervals, with no more than the maximum allowed number of animals in the bulk milk sample, in such a way that all lactating animals were tested in one of these samples. The p80 blocking ELISA (Priocheck BVDV antibody ELISA, Thermofisher, formerly CEDI Diagnostics) was used for antibody testing in serum and bulk milk. Using this blocking ELISA in a sample of five sentinel calves, a sensitivity of 96% and a specificity of 99.9% for detection of a within-herd prevalence of animals with BVDV antibodies of 70% was estimated (Mars and van Maanen, 2005). Data collection and study period Herd data were obtained from an automated certification administration system at GD Animal Health. All available test results of herds participating in the
Fig. 1. Flow chart of the bovine viral diarrhoea virus (BVDV)-free programme as practised in the Netherlands, with a test and cull phase in blue, a monitoring phase in green via antigen testing of newborn calves (option 1) or a spot test in young stock (option 2) and a removal phase for persistently infected animals (PIs) in red.
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60 ‘BVDV-free’ programme during the period 1 August 2007 to 1 August 2013 were included. To estimate the prevalence of active BVDV infection in dairy herds in The Netherlands, a random sample of dairy farms was selected out of a data set comprising all dairy farms with an unknown BVDV status using the ‘sample’ procedure in Stata/SE software version 14. Subsequently, farmers were invited to participate in a cross-sectional study in 2007 (n = 384), 2009 (n = 291) and 2011 (n = 287). Participating farmers were asked to have their private veterinary practitioner collect blood samples for a spot test. Herds with three or more positive samples were considered to have had recent BVDV circulation. The following descriptive results of the ‘BVDV-free’ programme during 20072013 are presented in this paper on a yearly basis: (1) the frequency distribution of spot test outcomes; (2) the percentage of herds that had two positive samples or a positive spot test (3 positive samples); (3) the spot test outcomes after a preceding favourable (negative) spot test; (4) the percentage of cohorts that had BVDV positive animals distributed per spot test category; (5) the spot test outcomes following favourable cohort testing; and (6) the age distribution of BVDV positive animals in cohort testing. In each of the parameters, censoring of herds, after leaving the programme, was taken into account.
Results Spot test During the study period, 31,975 spot tests were performed; of these spot tests, 98% (from 4857 unique herds) consisted of five blood samples collected from five animals per farm from 8–12 months of age and therefore were complete (Table 1). In 87% of these spot tests, no antibodies were detected, indicating no sign of BVDV circulation within the sampled group. In 8% of spot tests, only one animal was seropositive; this result did not lead to any further follow-up for the herd (Fig. 1). In 625 (2%) of spot tests, two samples tested positive for antibodies. This was considered to be an ambiguous result, so an extended spot test was required; resampling was performed in 482 (77%) of these herds (Fig. 2). The other herds either terminated their participation in the programme or did specific resampling in consultation with GD Animal Health, based on the suspicion of development of antibodies due to previous vaccination. Of these 482 herds, 192 had three or more seropositive calves at resampling and therefore cohort testing was commenced. This cohort testing was performed within 6 months in 141 herds; in 26 of these herds, at least one BVDV positive animal was found. In 4% of spot tests, antibodies were detected in three or more samples, indicative of BVDV circulation in the herd. In each year, an average of 6% of herds participating in the ‘BVDV-free’ programme had a spot test result that led to cohort testing in order to trace PIs on the farm. This percentage declined over time, while the number of herds participating in the ‘BVDV-free’ programme increased (Fig. 3). The number of seropositive animals in the initial spot test and in the spot test performed 6 months later (spot test +6 months) are presented in Table 2. At a spot test +6 months after a previous spot test with no seropositive animals, 3% of farms required cohort testing. At the spot test +6 months after a previous spot test with one seropositive animal, 8% of farms required cohort testing. At the
Table 1 Results of complete bovine viral diarrhoea virus spot tests (antibody testing of five animals aged 8–12 months) of 4857 unique herds collected in the period from 1 August 2007 until 1 August 2013. Number of seropositive calves
Number of spot tests
%
0 1 2 3 4 5 Total
27,115 2385 625 326 287 504 31,242
86.8 7.6 2.0 1.0 0.9 1.6 100
57
spot test +6 months after a previous spot test with two seropositive animals, 9% of farms required cohort testing (Table 2). Cohort testing BVDV positive animals were identified in 49% of herds that performed cohort testing. Cohort testing led to the detection of one or more virus positive animals in 18% of herds with two seropositive animals, 54% of herds with three or more seropositive animals and 68% if all five of the spot test samples were positive for antibodies against BVDV (Table 3). Twenty-eight percent of spot tests with three to five antibody positive samples were not followed by cohort testing within 6 months; reasons for this failure to follow-up included additional sampling because of antibodies due to vaccination or farmers terminating participation in the programme. No PIs were identified in 51% of herds in which cohort testing was performed; however, although no PIs were detected in these herds, more seropositive calves were detected in the spot test +6 months in these herds (Table 4) than in the overall total of all spot tests (Table 1). The more calves that were seropositive in the spot test preceding this negative cohort testing, the more calves were antibody positive in the spot test +6 months. If antibodies were detected in all five animals in the preceding spot test, but no PI was found, antibodies were also detected in five animals in 42% of spot test +6 months, whereas only 26% of spot tests +6 months that were preceded by five seropositive animals had no seropositive animals (Table 4). In 57% of this group, the spot test +6 months had three or more antibody positive animals, indicating virus circulation and therefore leading to repeated cohort testing. Confirmation testing A total of 1122 cohort tests were performed in 911 unique herds; of these, 522 herds had one or more BVDV positive animals. Within these positive cohort tests, 20,213 animals were tested for BVDV, of which 782 were positive. A birth date was available for 757 of these calves; BVDV positive animals were on average 6.8 months of age at the time of detection (Fig. 4). Two animals >20 months of age were BVDV positive; these animals were retested and were found to be transiently infected. Of the 522 herds in which BVDV positive animals were found after cohort testing, 90 (17%) performed confirmation testing; animals were resampled at the correct time point in 51/522 (57%) herds and virus was detected at resampling in 47/51 (92%) herds. At the animal level, 42% of retested animals were PIs; on average, these were 6.6 months old at the time of confirmation. Circulation of bovine viral diarrhoea virus among dairy herds with an unknown status The prevalence of herds with active BVDV infections among dairy herds with an unknown BVDV status was estimated to be 24% (95% confidence interval, CI, 19.5–28.3%), 23% (95% CI 18.3–28.3%) and 16% (95% CI 11.7–20.4%) in 2007, 2009 and 2011, respectively. In the same period the proportion of participants in the ‘BVDV-free’ and other BVDV control programmes increased from 23% to 39% (Fig. 5). Discussion Over a period of 20 years, experience was gained with a voluntary approach to BVDV control in the Netherlands. In the ‘BVDV-free’ programme, PIs were identified and culled, after which the BVDV status was monitored on the basis of the spot test. Data analysis over 6 years (1 August 2007 to 1 August 2013)
58
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60
Intake cattle Testing all Spot testfor virus (lactating animals in bulkmilk)
Intake cattle virus Testing Extenall ded spotfor test (lactating animals in bulkmilk)
Intake cattle for virus Testing allResult (lactating animals in bulkmilk)
Intake 0-2 seropositive animals Testing all cattle for virus (n = 290) (lactating animals in bulkmilk)
Intake Testing all cattlestatus for virus BVDV-free (lactating animals in bulkmilk)
2 seropositive animals in spot test ( n = 625)
3 or more seropositive animals (n = 192)
No BVD-virus (n = 115)
BVDV-free status
BVD-virus (n = 26)
Removal PI + 9 months virus testing
Cohort (n = 141)
Fig. 2. Flow chart of an extended spot test, after a spot test (antibody testing of five animals 8–12 months of age) with two animals being seropositive for antibodies against bovine viral diarrhoea virus (BVDV).
Fig. 3. Number of bovine viral diarrhoea virus (BVDV)-free herds monitored, based on spot testing in the ‘BVDV-free’ programme and the percentage of herds with a positive spot test.
Table 2 Results of bovine viral diarrhoea virus spot test (numbers and percentages of seropositive calves) 6 months after a previous spot test (spot test +6 months), with the preceding spot test having 0, 1 or 2 seropositive calves; spot tests with three or more seropositive animals lead to cohort testing. Preceding spot test
0 1 2
Spot test +6 months
Total
0
1
2
3
4
5
20,532 (90%) 1554 (78%) 286 (70%)
1412 (6%) 225 (11%) 60 (15%)
342 (1%) 72 (4%) 21 (5%)
173 (1%) 35 (2%) 14 (3%)
137 (1%) 38 (2%) 12 (3%)
242 (1%) 75 (4%) 13 (3%)
demonstrated that a voluntary programme can be successful, leading to an increasing number of ‘BVDV-free’ herds and a decrease in re-infection with BVDV in these herds. A single seropositive animal in the spot test may be caused by a false positive test result, vaccination induced antibodies or antibodies passively acquired via colostrum uptake (Fulton et al., 2004). In the Netherlands, vaccination is allowed and was implemented in a limited number of herds during the study period.
22,838 (100%) 1999 (100%) 406 (100%)
Since vaccine-induced antibodies may result in a positive spot test (Makoschey et al., 2007), it is advised to select unvaccinated animals for the spot test. A single seropositive animal in the spot test can also be caused by contact between animals infected with BVDV and the sampled age group, for example if a PI left the farm or died very young and therefore did not have the time to infect more animals in the herd (Houe, 1992). In the current ‘BVDV-free’ programme in the Netherlands, a follow up of a spot test with one
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60
59
Table 3 Percentage of cohorts with one or more bovine viral diarrhoea virus (BVDV) positive animals after two, three, four or five seropositive calves in the spot test. Number of seropositive calves
Number of herds required cohort testing
Number of herds that performed cohort testing <6 months
Percentage cohorts with BVDV positive animal (s)
2 3 4 5
192 326 287 504
141 201 190 416
18.4 29.9 49.5 67.8
Table 4 Distribution of bovine viral diarrhoea virus spot test results (numbers and percentages of seropositive calves) 6 months after a previous spot test (spot test +6 months), following negative cohort testing, as related to the number of positive calves in the preceding spot test. Preceding spot test
Spot test +6 months
2 3 4 5
45 56 30 22
0 (51%) (58%) (56%) (26%)
Total 1
2
19 (22%) 17 (18%) 6 (11%) 8 (10%)
8 4 4 6
3 (9%) (4%) (7%) (7%)
Fig. 4. Frequency distribution of the age of bovine viral diarrhoea virus (BVDV) positive animals in the ‘BVDV-free’ programme in the Netherlands during the period 2007–2013 at time of detection.
seropositive animal is advised, since cohort testing is costly and expenditures should be weighed against the chance of finding a PI. No BVDV positive animals were found in 51% of all cohorts tested. In these cohorts, animals that caused the spot test to be positive, by transmitting BVDV, may have been too young to be tested for BVDV, may have died at a young age (Duffell and Harkness, 1985) or may have left the farm for fattening (14–35 days after birth). Finding no PI does not mean that no BVDV infection occurred, as indicated by the subsequent spot test result, which had a higher than average chance of being positive. Thus, antibody detection indicates virus circulation in the herd, even if PIs are no longer present. Therefore, once a spot test is positive, it might be worthwhile advising farmers to test all newborn animals for BVDV (Fig. 1, option 1) in order to detect PIs as early as possible, instead of continuing with monitoring based on the spot test only. When the preceding spot test revealed two antibody positive animals, 70% of these herds had no seropositive animals in the spot test +6 months. Therefore, an additional sampling step was introduced, on the basis of which only 40% of these herds had to undertake cohort testing; this additional sampling thus prevented 60% of cohort testing (Fig. 2), considered to be economically worthwhile.
6 3 0 3
(7%) (3%) (0%) (4%)
4
5
3 (3%) 9 (9%) 7 (13%) 10 (12%)
7 (8%) 8 (8%) 7 (13%) 35 (42%)
88 97 54 84
(100%) (100%) (100%) (100%)
The detection of PIs at an average of 7 months of age is consistent with the biannual spot test frequency (Fig. 4). As a consequence, BVDV can be present in the herd for a relatively long period of time. A higher spot test frequency might reduce the age of animals in which PIs are found, thus reducing the chance of other animals in the herd becoming infected. Another way to find PIs at a younger age is by performing ear notch testing of newborn calves (Fig. 1, option 1). Single spot tests from randomly selected ‘non-participating’ dairy farms demonstrated that 16–24% of herds had active BVDV infections during the study period (Fig. 5). In the same period, the percentage of ‘BVDV-free’ farms having a positive spot test result was 6% per year on the basis of biannual testing. This shows that ‘BVDV-free’ herds have a lower risk of having BVDV circulation on their farm than farms with an unknown BVDV status. During the study period, the percentage of ‘BVDV-free’ herds with a positive spot test decreased from 7% (95% CI 6.0–8.1%) to 5% (95% CI 4.3– 5.8%) per year. The indication of BVDV circulation on dairy farms with an unknown BVDV status also declined from 24% (95% CI 19.5–28.3%) to 16% (95% CI 11.7–20.4%) during the study period. This decline may be caused by an increase in the proportion of participants in the ‘BVDV-free’ programme (Fig. 5), leading to a decrease in the number of PIs in the national cattle population. It is possible that herds with BVDV problems are more likely to participate in the ‘BVDV-free’ programme, in which case the remaining herds with an unknown BVDV status might be less likely to be BVDV positive. Other reasons for this decrease in prevalence could be further implementation of biosecurity measures (van Schaik et al., 2002) or an increase in the uptake of vaccination. Even though the prevalence of BVDV is declining, it will be difficult to eradicate BVDV from the Netherlands as long as not all farmers participate in a control programme, maintaining the risk of reintroduction (Santman-Berends et al., 2015). Eradication from the entire country would be facilitated by legislative support or industry pressure to introduce quality assurance schemes (Lindberg et al., 2006). Conclusions Analysis of the BVDV control programme in the Netherlands demonstrates that a voluntary programme can be successful, as suggested by an increasing number of ‘BVDV-free’ herds and a decrease in circulation of BVDV in these herds. The spot test, as well
60
L. van Duijn et al. / The Veterinary Journal 245 (2019) 55–60
Fig. 5. Distribution of dairy herds in different bovine viral diarrhoea virus (BVDV) categories: (1) ‘BVDV-free’ according to the ‘BVDV-free’ programme; (2) participating in any BVDV control programme but considered not to be ‘BVDV-free’; (3) BVDV status unknown by year in the period 2007–2013; and (4) percentage of herds with a positive spot test (antibody testing of five animals aged 8–12 months) in dairy herds with an unknown BVDV status in 2007, 2009 and 2011, with 95% confidence intervals.
as the combination of a spot test and extended spot test, is an efficient and effective tool to monitor the ‘BVDV-free’ status of a herd and to detect PI animals. Since 2007, the proportion of Dutch dairy herds with active BVDV infections has decreased, which may be related to the increasing number of participants in the ‘BVDVfree’ programme. Conflict of interest statement None of the authors has any financial or personal relationships that could inappropriately influence or bias the content of the paper. References Duffell, S.J., Harkness, J.W., 1985. Bovine virus diarrhoea-mucosal disease infection in cattle. Vet. Rec. 117, 240–245. Fulton, R.W., Briggs, R.E., Payton, M.E., Confer, A.W., Saliki, J.T., Ridpath, J.F., Burge, L. J., Duff, G.C., 2004. Maternally derived humoral immunity to bovine viral diarrhea virus (BVDV) 1a, BVDV1b, BVDV2, bovine herpesvirus-1, parainfluenza-3 virus bovine respiratory syncytial virus, Mannheimia haemolytica and Pasteurella multocida in beef calves, antibody decline by halflife studies and effect on response to vaccination. Vaccine 22, 643–649. Gaede, W., Gehrmann, B., Korber, R., 2003. Viramikereliminerung: Effektives herdenscreening durch kombination von RT-PCR und antigen-ELISA in blutund milchproben. Berl. Munch. Tierarztl. Wochenschr. 116, 234–239. Graham, D.A., Lynch, M., Coughlan, S., Doherty, M.L., O’Neill, R., Sammin, D., O’Flaherty, J., 2014. Development and review of the voluntary phase of a national BVD eradication programme in Ireland. Vet. Rec. 174, 67. Greiser-Wilke, I., Grummer, B., Moennig, V., 2003. Bovine viral diarrhoea eradication and control programmes in Europe. Biologicals 31, 113–118.
Houe, H., 1992. Serological analysis of a small herd sample to predict presence or absence of animals persistently infected with bovine viral diarrhoea virus (BVDV) in dairy herds. Res. Vet. Sci. 53, 320–323. Lindberg, A., Brownlie, J., Gunn, G.J., Houe, H., Moennig, V., Saatkamp, H.W., Sandvik, T., Valle, P.S., 2006. The control of bovine viral diarrhoea virus in Europe: today and in the future. Rev. Sci. Tech. 25, 961–979. Lindberg, A., Houe, H., 2005. Characteristics in the epidemiology of bovine viral diarrhea virus (BVDV) of relevance to control. Prev. Vet. Med. 72, 55–73. Makoschey, B., Sonnemans, D., Bielsa, J.M., Franken, P., Mars, M.H., Santos, L., Alvarez, M., 2007. Evaluation of the induction of NS3 specific BVDV antibodies using a commercial inactivated BVDV vaccine in immunization and challenge trials. Vaccine 25, 6140–6145. Mars, M.H., van Maanen, C., 2005. Diagnostic assays applied in BVDV control in The Netherlands. Prev. Vet. Med. 72, 43–48. Norstrom, M., Jonsson, M.E., Akerstedt, J., Whist, A.C., Kristoffersen, A.B., Sviland, S., Hopp, P., Wahlstrom, H., 2014. Estimation of the probability of freedom from bovine virus diarrhoea virus in Norway using scenario tree modelling. Prev. Vet. Med. 116, 37–46. Presi, P., Heim, D., 2010. BVD eradication in Switzerland — a new approach. Vet. Microbiol. 142, 137–142. Presi, P., Struchen, R., Knight-Jones, T., Scholl, S., Heim, D., 2011. Bovine viral diarrhea (BVD) eradication in Switzerland — experiences of the first two years. Prev. Vet. Med. 99, 112–121. Reichel, M.P., Lanyon, S.R., Hill, F.I., 2016. Moving past serology: diagnostic options without serum. Vet. J. 215, 76–81. Santman-Berends, I.M., Mars, M.H., van Duijn, L., van Schaik, G., 2015. Evaluation of the epidemiological and economic consequences of control scenarios for bovine viral diarrhea virus in dairy herds. J. Dairy Sci. 98, 7699–7716. Stahl, K., Alenius, S., 2012. BVDV control and eradication in Europe — an update. Jpn. J. Vet. Res. 60 (Suppl), S31–S39. van Schaik, G., Schukken, Y.H., Nielen, M., Dijkhuizen, A.A., Barkema, H.W., Benedictus, G., 2002. Probability of and risk factors for introduction of infectious diseases into Dutch SPF dairy farms: a cohort study. Prev. Vet. Med. 54, 279–289. Walz, P.H., Grooms, D.L., Passler, T., Ridpath, J.F., Tremblay, R., Step, D.L., Callan, R.J., Givens, M.D., 2010. Control of bovine viral diarrhea virus in ruminants. J. Vet. Intern. Med. 24, 476–486.