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MINISTRY OF AGRICULTURE, FISHERIES AND FOOD CSG 15Research and Development

Final Project Report(Not to be used for LINK projects)

Two hard copies of this form should be returned to:Research Policy and International Division, Final Reports UnitMAFF, Area 6/011A Page Street, London SW1P 4PQ

An electronic version should be e-mailed to [email protected]

Project title The epidemiology and economics of BVD virus infection in BVD virus naïve dairy herds

MAFF project code OD 0339

Contractor organisation and location

Veterinary Laboratories Agency WeybridgeWoodham LaneNew Haw, AddlestoneSurrey KT15 3NB

Total MAFF project costs £ 149,370

Project start date 01/01/98 Project end date 31/03/01

Executive summary (maximum 2 sides A4)

Bovine viral diarrhoea virus (BVDV) is probably the most economically important viral disease of cattle in the developed world including the UK. It has a complex natural history and causes a wide range of losses in affected herds including repeat breeding, abortion, foetal abnormalities, drop in milk production, immunosuppression and deaths. Cattle may also be subclinically infected with BVDV. Possible control measures include identification and removal of cattle persistently infected with BVDV from herds, implementation of strict biosecurity precautions and since 1996, vaccination.

Because of the complex effects of BVDV infection and the range of control measures available, studies using various economic decision-making techniques have been used to advise farmers, industry and government on the cost-effective control of BVDV. These studies showed that there is a paucity of good quality data on the risk of occurrence of BVDV infection and its various effects, and on the expected losses in herds under different conditions. In this project, our main aim was to provide reliable data on the incidence of BVDV infection and its effects in BVDV naïve dairy herds in England, which could be used in the economic evaluation of BVDV control options.

The specific objectives of the project were

(a) to determine the annual incidence of BVDV infection in BVDV naïve dairy herds,(b) to determine the source(s) of BVDV infection in BVDV naïve dairy herds that became infected with BVDV,

and (c) to estimate the losses that occurred in BVDV naïve dairy herds that become infected with BVDV.

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Projecttitle

The epidemiology and economics of BVD virus infection in BVD virus naïve dairy herds

MAFFproject code

OD 0339

To identify BVDV naive herds for the study, bulk tank milk samples from 394 herds recorded on the DAISY dairy information system were screened for BVDV antibodies using an indirect ELISA. Herds with an optical density ratio of less than 0.35 were considered BVDV naive. Forty BVDV naive herds were recruited into the study in August 1998 and their BVDV status was monitored for two years by two-monthly testing of bulk tank milk for BVDV antibodies. Herds in which BVDV infection was suspected were investigated to determine the most likely source of the infection. At the end of the monitoring period, the reproductive and productive performance of the herds that became infected with BVD virus was compared with that in the herds that remained free from BVDV infection. The risk of a BVDV naïve herd becoming infected with BVDV was also calculated.

The prevalence of DAISY herds considered BVDV antibody positive was 96 per cent and 65 per cent of the herds screened had a high level of BVDV antibody. This level of exposure to BVDV was virtually the same as that found in a 1996 survey of 1070 dairy herds in England and Wales.

The risk of a herd experiencing a BVDV breakdown over the course of a year was around 10 to 11 per cent. The incidence rate of BVDV herd breakdowns was lower than anticipated and may have been due to increased farmer awareness of BVD. At the end of 1996, a BVD vaccine was marketed in the UK for the first time. An interesting feature of the study was the fall in the annual incidence rate of BVDV herd breakdowns in each of the three years of the study. It is likely that the regular monitoring of their herds for BVDV stimulated farmers to take a more active role in preventing the virus entering their herds. If this was the case, the use of bulk milk tests to monitor endemic infections on dairy farms could be a powerful tool to improve biosecurity on farms.

Purchased cattle appear to have been responsible for introducing BVDV infection into five of the 10 BVDV breakdown herds. However, in one of these herds, a neighbour’s bull, which broke in and served a cow, may have introduced BVDV into the herd. The BVDV breakdown in a sixth herd may have been caused by the unexplained return to the herd of a cow that had been sold for slaughter six weeks earlier. The cow may have become infected with BVDV while off the farm. In the remaining four herds, no obvious source of BVDV infection was found. The study confirmed the importance of purchased cattle as a source of BVDV infection for BVDV naïve herds and the necessity to test these animals for BVDV before they join the herd. The testing should also include purchased and hired or shared bulls. In the study, bulls were implicated as a source of BVDV infection in two herds.

No statistically significant difference was found between the reproductive performance, disease outcomes, milk yield and somatic cell counts of the BVDV breakdown herds and the herds that remained BVDV naïve. The most likely reason for these results was the small sample size. However, some results did suggest an adverse effect due to the disease. The abortion rate, per cent of calves born dead and mortality rate were slightly higher in the BVDV breakdown herds. Average annual somatic cell counts were also higher in the BVDV breakdown herds.

No further work on quantifying the losses caused by BVDV is proposed. Since this project was conceived in 1997, an effective BVDV vaccine has became available in the UK. Because the vaccine is expensive, studies which compare the losses between vaccinated and unvaccinated cows on the same farms have been carried out to demonstrate its cost-effectiveness. New computer models have also been developed to explore the cost-effectiveness of different BVDV control options on farms.

When the project started, there was concern about the possibility that the UK might have to follow other EU countries in eradicating BVDV from its national herd. Given the high level of BVDV infection in the UK, there was uncertainty about whether there would be an economic benefit from pursuing the eradication option. In the future, a cost-benefit analysis of a national eradication programme for BVDV could prove useful to inform government policy in this area.

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Projecttitle


MAFFproject code

OD 0339

Scientific report (maximum 20 sides A4)Epidemiology and economics of BVD virus infection in BVD virus naive dairy herds

K. H. Christiansen1, M. A. Kossaibati2, R. J. Esslemont2

1Veterinary Laboratories Agency Weybridge, New Haw, Addlestone, Surrey KT15 3NB2The University of Reading, Department of Agriculture, Earley Gate, Reading RG6 6AT

INTRODUCTION AND OBJECTIVES

Bovine viral diarrhoea virus (BVDV) is probably the most economically important viral disease of cattle in developed countries including the UK (Donis and others 1991). Around 60% of cattle and 90 to 95% of herds in England and Wales are infected with BVDV (Harkness and others 1978, Paton and others 1998).

Cattle of all ages are susceptible to acute infection with BVDV. Acute BVD is usually an inapparent to mild disease of short duration, high morbidity and negligible mortality. However, outbreaks of severe acute enteritis with significant mortality and a drop in milk yield do occur occasionally in adult cattle (Pritchard and others 1989, David and others 1994). There is also evidence that acute infection of calves with BVDV may have an immunosuppressive effect on the host and so potentiate the effect of other infectious diseases, such as pneumonia (Stott and others 1980).

BVDV infection of susceptible pregnant cattle almost invariably results in the transfer of the virus to the foetus. The outcome may be an aborted or stillborn foetus or the birth of a congenitally malformed calf, a weak, undersized calf or a clinically normal calf (Done and others 1980). Infection of susceptible cows at the time of breeding can cause early embryo loss and repeat breeding (McGowan and others 1993). Foetal infection with BVDV in early gestation induces specific immunotolerance to the virus (McClurkin and others 1984). Such calves are born persistently infected (PI) with BVDV and shed large amounts of the virus for life while remaining antibody negative (Brownlie and others 1984). They are frequently ill-thrifty and have a high probability of developing fatal mucosal disease, which commonly occurs between 6 and 18 months of age. Calves born from PI cows are always persistently infected.

Persistently infected animals play a key role in perpetuating BVDV infection in cattle populations and their identification and removal from herds is considered an important control strategy for the disease. Other control strategies include implementing strict biosecurity measures and increasing herd immunity through vaccination or deliberate exposure to PI animals (Brownlie and others 1995, Harkness 1987).

Because of the complex effects of BVDV infection and the range of control measures available, various economic decision-making techniques have been used to advise industry and government on the cost-effective control of BVDV. In the UK, Bennett and Done (Bennett and Done 1986, Bennett and Done 1987) explored the use of cost-benefit analysis and decision-tree analysis to evaluate control strategies for BVDV at the national and farm levels respectively. In Denmark, decision-tree analysis (Houe and others 1994) and simulation modelling (Sorensen and others 1995) were used to evaluate control strategies for BVDV. All these studies showed that there is a paucity of good quality data on the risk of occurrence of BVDV infection and its various effects, and on the expected losses in herds under different conditions. Sorensen and others (1995), in using data from a BVDV outbreak in a British herd (Duffell and others 1986), showed that data on losses due to BVDV in individual herds are useful to validate economic models. However, case reports that provide usable information on disease losses are rare for most diseases, including BVDV.

In this project, our main aim was to provide reliable data on the incidence of BVDV infection and its effects in BVDV naïve dairy herds in England, which could be used in the economic evaluation of BVDV control options. The project design also provided the opportunity to investigate the source of BVDV for each newly infected herd. The purchase of a PI animal or a pregnant animal carrying a PI foetus is considered the most

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Projecttitle


MAFFproject code

OD 0339

common cause of a BVDV outbreak in a herd, but other potential sources include contact with acutely infected cattle, with infected sheep and goats, semen, embryo transfer and needle transmission (Houe 1995). The aim was to determine the relative importance of the various sources of BVDV infection for dairy herds in England.

The specific objectives of the project were

(a) to determine the annual incidence of BVDV infection in BVDV naïve dairy herds,

(b) to determine the source(s) of BVDV infection in BVDV naïve dairy herds that became infected with BVDV, and

(c) to estimate the losses that occurred in BVDV naïve dairy herds that become infected with BVDV.

MATERIALS AND METHODS

Overview

The BVDV status of 40 BVDV naive dairy herds was monitored for two years by regular testing of bulk tank milk for BVDV antibodies. Herds in which BVDV infection was suspected were investigated to determine the most likely source of the infection. At the end of the monitoring period, the reproductive and productive performance of the herds that became infected with BVD virus was compared with that in the herds that remained free from BVDV infection.

Herd selection

In order to identify BVDV naive herds for the study, bulk tank milk samples from 414 herds recorded on the DAISY dairy information system were screened for BVDV antibodies using an indirect ELISA. The methodology and results of the survey have been described previously (Kossaibati and others 2000). All herds were located in England and were tested for BVDV antibodies between February and June 1998.

Herds with a BVDV antibody ELISA optical density (OD) ratio of less than 0.35 were considered BVDV naive. When herds that had been vaccinated against BVD were excluded from the analysis, 52 (13 per cent) of 394 herds met the criterion for a BVDV naive herd. Forty-four farmers with BVDV naive herds agreed to participate in the two-year follow-up study. However, in the first three months, two farmers withdrew from the study, one herd was sold and two herds were amalgamated to give a final sample size of 40 herds.

Bulk milk monitoring

To detect infection of the study herds with BVDV, bulk tank milk samples from the 40 herds were tested for BVDV antibodies at approximately two-monthly intervals between August 1998 and November 2000. All bulk milk samples were tested by the Veterinary Laboratories Agency Langford using the antibody ELISA as described for the screening test (Kossaibati and others 2000). The bulk milk samples were collected by veterinary surgeons or farmers, who used sampling kits supplied by the project (Kossaibati and others 2000). Each sample was accompanied by a laboratory submission form giving the number of cows in the dairy herd, number of cows contributing milk to the bulk tank on sampling day, whether the farmer had bought in any cattle since the last bulk milk test, and whether the herd had been vaccinated against BVD since the last bulk milk test.

BVDV herd breakdowns

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Projecttitle


MAFFproject code

OD 0339

A BVDV naïve herd was considered likely to have become infected with BVDV if, on two consecutive bulk milk BVDV antibody ELISAs, it had an OD ratio greater than 0.34 (that is, class 2 or 3) and the OD ratio was at least double the minimum BVDV antibody OD ratio recorded for the herd to date. A further criterion was that no cows in the milking herd had been vaccinated against BVDV in the four months before the rise in OD ratio. No attempt was made to confirm that animals in a BVDV breakdown herd were actively infected with BVDV through the use of the BVDV antigen ELISA or RT-PCR.

The BVD OD class is a system developed by Scandinavian researchers to relate the bulk milk BVDV antibody ELISA level to the likely proportion of sero-positive cows in the milking herd (Lindberg 1995). The OD ratios that equate to these classes are as follows:

Class 0 = OD ratio of <0.1, indicating that <5% of milking cows are likely to be sero-positive. Class 1 = OD ratio of 0.1 - 0.34, indicating approximately 5 - 25% of sero-positive milkers.Class 2 = OD ratio of 0.35 - 0.7, indicating approximately 25 - 65% of sero-positive milkers.Class 3 = OD ratio of >0.7, indicating >65% of sero-positive milkers.

Incidence rates

Two types of incidence rate were used to express the rate of occurrence of BVDV breakdowns in BVDV naive dairy herds.

The cumulative incidence rate or risk rate is the proportion of BVDV naive herds at the beginning of the stated time period that had a BVDV breakdown during that time period. It represents the average risk or probability that a BVDV naive herd will have a BVDV breakdown during a particular time period.

To determine the average annual risk rate of BVDV herd breakdowns from the risk rate calculated for the full period of observation of the study herds, the following formula was used (Martin and others 1987):

Risk rate in y months = 1 – (1 – risk rate in x months) y/x The incidence density rate or true incidence rate was used to describe the average speed at which BVDV breakdowns occurred per month of herd time at risk (Martin and others 1987). It was defined as:

Number of BVDV breakdowns that occurred in the study herds during a stated period of time The sum, over all herds, of the length of time at risk of having a BVDV breakdown

The cumulative incidence rate can be estimated from the incidence density rate using the following formula (Thrusfield 1995):

Cumulative incidence rate = 1 – e -incidence density rate

Investigation of BVDV breakdown herds

At the start of the project, all farmers completed a general questionnaire describing the herd and its management. To determine the most likely source of BVD virus infection in a BVDV breakdown herd, a detailed epidemiological investigation of the herd was carried out by the farmer’s veterinary surgeon and one of the project researchers (MK). Information about possible sources of BVD virus infection for the dairy herd was collected using a standard questionnaire. The BVDV herd breakdown questionnaire comprised three sections:

Part A. Farm Management Practices sought information from the farmer about management practices that may have led to the introduction of BVD virus into the dairy herd. Questions were asked about cattle purchases, contact among groups of cattle on the farm and with cattle on other farms, contact with other

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Projecttitle


MAFFproject code

OD 0339

animal species that might carry BVDV (sheep, deer) and the use of AI, hired or shared bulls and embryo transfer.

Part B. Current BVD Testing and Disease History summarised BVD testing and disease information related to the current BVDV breakdown. In many cases, additional testing information, past and present, was supplied by the farmer’s veterinary surgeon and recorded on the questionnaire.

Part C. Source of BVD Virus Infection for the Dairy Herd asked for the veterinary surgeon’s opinion about the most likely source of BVD virus infection for the dairy herd.

Epidemiological information about the cause of the BVDV breakdown was supplemented with a limited amount of laboratory testing of individual cattle in the herd. The following tests were undertaken free of charge to the farmer:

(a) BVDV antibody ELISA on individual milk samples from six first lactation, homebred cows.

(b) BVDV antibody ELISA on individual milk samples from up to six cows that were added to the milking herd during the four months before the bulk milk test at which the herd was declared a BVDV breakdown. These cows could be newly purchased animals or dry cows but first lactation homebred cows were excluded.

(c) BVDV antibody ELISA on individual clotted blood samples from six homebred young stock (dairy replacement heifers) aged between 8 and 15 months. A preference for cattle at the lower end of this age range was indicated.

The broad conclusions drawn from the battery of tests carried out on the BVDV breakdown herds are given in Table 1 (Adapted from Pritchard 1998). The results were interpreted in conjunction with the increase in bulk milk BVDV antibody level, which suggested that the prevalence of sero-positive cows in the milking herd had risen significantly. Milk and blood samples from individual animals were considered negative if the BVDV antibody OD ratio was <0.2.

TABLE 1: Interpretation of battery of BVDV antibody tests carried out on groups of cattle in BVDV breakdown herds

First lactation homebred cows

Cows recently added to the milking herd

8 to 15 month old homebred heifers

Interpretation

All negative All negative All negative Probably no active infectionAll negative Some or all positive All negative Probably no active infection. Cows with

high antibody levels added to the herdAll negative All negative or some

or all positiveSome or all positive

Persistently infected cattle probably present among young stock

Some or all positive

All negative or some or all positive

All negative Active infection (acute or persistently infected) in milking herd


All negative or some or all positive


Active infection in milking herd. Persistently infected cattle probably present among young stock

Collection and analysis of reproduction, health and milk production data

Reproduction, health and milk production data for the study herds were obtained mainly from the DAISY dairy information system. Although herds entering the study had to be on DAISY, by the end of the study, some farmers had changed to other herd recording systems. Where possible, data from non-DAISY systems were collated into DAISY format. Reproduction, health and milk production data were obtained over the two-

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Projecttitle


MAFFproject code

OD 0339

year bulk milk monitoring phase and for the year before bulk milk monitoring commenced. The recording year for the data ran from 1 July to 30 June of each year. Only data that were routinely recorded for herds on the DAISY dairy information system were collected.

The losses due to BVDV infection in BVDV naïve dairy herds were determined by comparing the mean reproductive and productive performance in herds that became infected with BVDV with that in the uninfected herds using Student’s t-test.

RESULTS

BVD bulk milk survey of DAISY herds

The results of the BVD bulk milk survey, which was carried out to identify BVDV naive herds for the study, have been described previously (Kossaibati and others 2000). Briefly, valid data were available for 394 of the 414 DAISY herds that were screened for BVDV antibodies. Nearly 60 per cent of the 394 herds were located in the South West region. No herds from East Anglia were included in the survey. The average number of cows in these herds was 123 (range 25 to 435 cows) and the mean number of cows contributing to the tank when the sample was taken was 108 (range 20 to 360 cows). Forty-two per cent of farmers had bought in cattle during the year before the bulk milk sample was collected.

The overall mean level of BVDV antibodies in bulk tank milk samples from the 394 herds was 0.79 (range 0.0 to 1.47). Dairy herds in the South East region had a significantly lower mean BVDV OD ratio than dairy herds in the rest of England (Table 2). The percentages of herds in each BVDV antibody class are shown in Table 2. The prevalence of herds considered BVDV antibody positive (Classes 1, 2 and 3) was 95.7 per cent and the prevalence of those considered BVDV naive (Classes 0 and 1) was 13.2 per cent. Most herds (67%) had a high level of BVDV antibody in the bulk milk.

TABLE 2: Mean level of BVDV antibodies in bulk milk samples and number and per cent of dairy herds in each BVDV class in England and by region

Region No. of herds

% of total

herds

Mean BVDV OD

ratio

No. (%) of herds in Class 0




North 23 5.8 0.93 0 (0.0) 0 (0.0) 5 (21.7) 18 (78.3)

North West 6 1.5 0.97 0 (0.0) 0 (0.0) 1 (16.7) 5 (83.3)Yorks & Humberside 33 8.4 0.83 2 (6.1) 2 (6.1) 6 (18.2) 23 (69.7)East Midlands 13 3.3 0.79 0 (0.0) 2 (15.4) 3 (23.1) 8 (61.5)West Midlands 46 11.7 0.87 0 (0.0) 4 (8.7) 8 (17.4) 34 (73.9)South East 46 11.7 0.61 7 (15.2) 8 (17.4) 10 (21.7) 21 (45.7)South West 227 57.6 0.79 8 (3.5) 19 (8.4) 45 (19.8) 155 (68.3)

England 394 100.0 0.79 17 (4.3) 35 (8.9) 78 (19.8) 264 (67.0)

The mean BVDV OD ratio in herds where the farmer had bought in cattle over the year before the test was 0.87. This was significantly higher than the mean BVDV OD ratio of 0.74 in herds where cattle were not purchased (P<0.01). Forty-five per cent of farmers with a Class 2 or 3 herd had purchased cattle compared with 25% of farmers with a BVDV naive herd (Class 0 or 1). Herd size and the number of cows contributing milk to the bulk tank on sampling day had no significant effect on bulk milk BVDV antibody levels.

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Projecttitle


MAFFproject code

OD 0339

Bulk tank milk monitoring of BVDV naïve herds

Twenty-two of the 40 BVDV naive dairy herds in the study were located in the South West region. The regional distribution of the remaining herds was as follows: South East - 7 herds, West Midlands - 4 herds, East Midlands - 3 herds, Yorkshire and Humberside - 4 herds. The average number of milking cows in the 40 herds was 118 (median 114, range 37 to 250).

A total of 373 BVDV antibody ELISA tests were carried out on the 40 herds over the bulk milk monitoring phase. At the initial screening test, 12 herds were placed in BVD OD Class 0 and 28 herds were in BVD OD Class 1. At the end of the study, three herds had remained in Class 0 throughout the monitoring phase. Eighteen herds had at least one bulk milk test result in Class 1, 10 herds had at least one bulk milk test result in Class 2 and nine herds had at least one bulk milk test result in Class 3. The mean OD level across all herds over the study period was 0.24. The average number of cows contributing milk to the bulk tank at the time of sampling was 99. Thirteen farmers bought in one or more cattle over the study period. Ten herds met the study definition of a BVDV breakdown and seven of the 10 farmers with BVDV breakdown herds vaccinated their cattle against BVD after the breakdown. Detailed results are shown in Table 3.

TABLE 3: BVD status and herd characteristics of 40 BVDV naive dairy herds over the study period (February 1998 to October 2000)

Min. OD

Class

Max. OD

Class

No. of herds

Mean (SD) OD ratio1

Range of OD ratios

Mean no. milking cows

Mean no. cows in milk2

No. with purchased cattle

No. given BVD

vaccine

No. BD

herds3

0 0 3 0.02 (0.03) 0.00-0.08 88 75 0 0 00 1 16 0.08 (0.07) 0.00-0.27 128 108 4 0 01 1 2 0.21 (0.06) 0.15-0.30 121 100 0 0 00 2 2 0.17 (0.13) 0.00-0.39 92 74 0 0 11 2 8 0.34 (0.13) 0.12-0.67 115 97 1 1 10 3 4 0.40 (0.27) 0.00-1.12 124 101 3 3 31 3 5 0.58 (0.29) 0.12-1.14 115 96 5 3 5

All herds

40 0.24 (0.24) 0.00-1.14 118 99 13 7 10

1SD = standard deviation2Mean number of cows contributing milk to the bulk tank at time of sampling3Number of herds meeting the study definition of a BVDV breakdown herd

Incidence of BVDV breakdowns

Between 1 February 1998 and 31 October 2000, ten (25%) of the 40 BVDV naive dairy herds in the study had a BVDV breakdown. Assuming a constant rate of BVDV breakdowns over the 33-month period, the annual risk rate of BVDV herd breakdowns was 9.9 per cent. In the first year of observation, the risk of a BVDV naive herd having a BVDV breakdown was 12.5 per cent. In the second year of observation, the risk rate was 11.4 per cent and in the last 9 months of the study, it was 3.2 per cent.

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Projecttitle


MAFFproject code

OD 0339

The true incidence rate of BVDV breakdowns in the 40 BVDV naive dairy herds was 11.8 per 100 herd-years at risk. In the first year of observation, the true incidence rate was 13.0 per 100 herd-years at risk. In the second year of observation, the true incidence rate was 12.2 per 100 herd years at risk and in the third year, it was 7.3 per 100 herd-years at risk.

When the true incidence rate was used to estimate the risk of a BVDV naive herd having a BVDV breakdown, the average annual risk rate was 11.1 per cent. The estimated risk rate fell from 12.2 per cent in year 1 to 11.5 per cent in year 2 and 7.1 per cent in year 3.

Source of BVDV infection in the BVDV breakdown herds

Possible sources of BVDV infection for the ten dairy herds that had a BVDV breakdown are summarised in Table 4. Purchased cattle appear to have been responsible for introducing BVDV infection and/or cows or heifers with high BVDV antibody titres into five of the 10 herds (herds 2, 9, 13, 29, 31). However, in one of these herds (herd 29), a neighbour’s bull, which broke in and served a cow, may have introduced BVDV into the herd. The BVDV breakdown in herd 42 may have been caused by the unexplained return to the herd of a cow that had been sold for slaughter six weeks earlier. The cow may have become infected with BVDV while off the farm. In the remaining four herds (herds 23, 28, 35, 44), no obvious source of BVDV infection was found. There was doubt about whether herds 28 and 35 were actively infected with BVDV, while herd 44 may have been infected before the project began.

Losses in BVDV naïve dairy herds that became infected with BVDV

(a) Fertility data

No reproduction data were available for BVDV breakdown herds 29 and 44 and for control herds 7, 32, 33 and 39. The data were summarised only for year 1 of the monitoring phase (1 July 1998 to 30 June 1999) because data for year 2 (1 July 1999 to 30 June 2000) were incomplete when data collection closed on 31 December 2000. Therefore, only herds that had a BVDV breakdown before the 30 June 1999 were included in the analysis. These were herds 9, 13, 23 and 28. Two herds whose data were recorded on non-DAISY systems did not have data for all the variables of interest. One herd was a BVDV breakdown (herd 13) and the other herd was a control (herd 35). (Note that herd 35 was a case herd in year 2.)

The mean reproductive performance in the four herds that became infected with BVDV in year 1 was compared with that in the 30 herds that were BVDV-naïve in year 1 (Table 5). There was no statistically significant difference between the BVDV breakdown herds and the control herds in any of the reproductive performance parameters.

TABLE 4: BVDV antibody ELISA levels in bulk milk and likely reasons for BVDV breakdowns in BVDV naïve dairy herds

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Projecttitle


MAFFproject code

OD 0339

Herdno.

Date of breakdow

n (BD)

Initial bulk milk OD ratio

Bulk milk OD ratio at date of BD

Likely reason for bulk milk BVDV antibody rise at which herd was classed as a BVDV breakdown

Likely reason for BVDV infection entering the herd

23 31/08/98 0.00 0.99 Addition to the milking herd of the first lactation cows, that probably were transiently infected with BVDV before they joined the milking herd.

No obvious source of BVDV infection for the first lactation cows.

29 15/09/98 0.21 0.48 Active BVDV infection in the milking herd.

1.Neighbour’s bull that broke in and served a cow. 2. Purchased cattle.

28 18/11/98 0.27 0.65 Addition to the milking herd of cows with high BVDV antibody titres from past exposure.

No obvious source of BVDV infection, whether recent or past.

9 14/12/98 0.12 0.68 Addition to the milking herd of first lactation cows that had been purchased as calves and had high BVDV antibody titres.

Purchase of BVDV infected bull.

13 29/12/98 0.32 0.73 Addition to the milking herd of recently purchased heifers that had high BVDV antibody titres.

Purchase of BVDV infected heifers.

44 12/06/99 0.27 0.58 Addition to the milking herd of cows with high BVDV antibody titres from past exposure and/or active infection in milking herd.

Milking herd may have been actively infected with BVDV before the project started. Source unknown.

35 30/06/99 0.20 0.46 Addition to the milking herd of cows with high BVDV antibody titres from past exposure.

No evidence of active BVDV infection in the milking herd.

2 06/08/99 0.20 0.76 Addition to the milking herd of recently purchased heifers that had high BVDV antibody titres.

Purchase of BVDV infected heifers.

42 01/11/99 0.07 0.39 Active BVDV infection in the milking herd.

Accidental return to the herd after six weeks of a cow that was sold for slaughter. Cow may have become infected with BVDV while off the farm but not confirmed.

31 09/10/00 0.29 1.08 Active infection in the milking herd together with addition to the milking herd of purchased heifers with high BVDV antibody titres

Purchase of an in-calf heifer persistently infected with BVDV.

TABLE 5: Comparison of fertility variables in four BVDV breakdown herds (case herds) and 26 BVDV naïve herds (control herds) in year 1 (1998/99) of the study

Variable Case herds Control herds P-valueNo. Mean No. Mean

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Projecttitle


MAFFproject code

OD 0339

Average number of heifers and cows calved 4 115.5 30 129.2 0.63Per cent served of calved 4 82.7 30 87.2 0.12Average calving to first service interval (days) 4 84.5 30 76.5 0.55*

Average first service 24-day submission rate (%) 3 47.7 29 44.2 0.52Average first service pregnancy rate (%) 3 47.0 29 46.2 0.87Average all services pregnancy rate (%) 4 52.5 30 47.3 0.87*

Average % conceived of served 4 91.2 30 89.2 0.38Average % conceived of calved 4 77.2 30 79.0 0.61Average calving to conception interval (days) 4 110.2 30 107.6 0.98*

Average days open 3 138.3 29 138.4 1.00Average number of services per conception 4 1.9 30 2.0 0.35Average lactation (days) 4 344.7 30 324.4 0.13Average calving interval (days) 4 395.7 30 389.0 0.87*

Per cent culled of calved 4 21.5 30 21.4 0.99*Kruskal-Wallis test was used because the sample variances were not homogeneous

(b) Health data

Reliable health data were available only for year 1 of the monitoring phase (1 July 1998 to 30 June 1999). Therefore, only herds that had a BVDV breakdown before the 30 June 1999 were included in the analysis. These were herds 9, 13, 23, 28, 29 and 44. No data were available for control herd 39 and for some health variables, data were also missing for control herds 7, 8, 12, 14, 17, 30, 31 and 32.

The prevalence of various health conditions in the six herds that became infected with BVDV in year 1 was compared with that in the herds that were BVDV-naïve in year 1 (Table 6). Generally, the health status of the control herds was lower than that of the case herds. However, the per cent of calves born dead, abortion rate and mortality rate were higher in the BVDV breakdown herds although the difference was not statistically significant.

(c) Milk yield and somatic cell count

Milk yield and somatic cell count data were available for 33 of the 40 herds in the study. The data were summarised for the years 1 July 1998 to 30 June 1999 (year 1) and 1 July 1999 to 30 June 2000 (year 2). Four herds (9, 13, 23, 28) had a BVDV breakdown in year 1 and a further four herds (2, 31, 35, 42) had a BVDV breakdown in year 2.

The mean reproductive performance in the four herds that became infected with BVDV in year 1 was compared with that in the 30 herds that were BVDV-naïve in year 1 (Table 7). There was no statistically significant difference between the case and control herds in milk yield, milk composition or somatic cell count. However, the somatic cell count was higher in the BVDV breakdown herds, especially in year 2 of the study.

TABLE 6: Comparison of health variables in six BVDV breakdown herds (case herds) and 33 or 25 BVDV naïve herds (control herds) in year 1 (1998/99) of the study

Variable Case herds Control herds P-valueNo. Mean No. Mean

Per cent of cows with difficult calving 6 5.8 33 7.1 0.73Per cent of cows with twins 6 3.5 33 3.5 0.71*

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MAFFproject code

OD 0339

Per cent of calves born dead 6 7.1 33 6.4 0.77*

Per cent of cows aborting 6 0.9 33 0.6 0.51Per cent of cows with retained foetal membranes 6 1.2 33 3.9 0.06*

Per cent of cows with milk fever 6 2.7 33 4.3 0.30Average number of mastitis cases per 100 cow-years 6 20.9 25 47.7 0.13*

Average number of lameness cases per 100 cow-years

6 7.5 25 18.7 0.14

Average number of oestrus-not-observed cases per 100 cow-years

6 35.2 25 53.5 0.36

Average number of cases of vulval discharge per 100 cow-years

6 1.2 25 12.2 0.02*

Culling rate (%) 6 17.6 25 25.1 0.14Mortality rate (%) 6 1.9 25 1.2 0.39

*Kruskal-Wallis test was used because the sample variances were not homogeneous

TABLE 7: Comparison of annual milk yield and somatic cell counts in BVDV breakdown herds (case herds) and BVDV naïve herds (control herds) in year 1 and year 2 of the study

Variable Year in which Year of Case herds Control herds P-valuevariable was

measuredherd

breakdownNo. Mean No. Mean

Annual milk yield (kg/cow/year)

1222

112

1 & 2

4448

8206842177958108

29252525

8140805580558055

0.900.510.23*

0.89Fat % 1

222

112

1 & 2

4448

4.0504.0753.7753.925

29252525

3.9243.9083.9083.908

0.270.190.340.87

Protein % 1222

112

1 & 2

4448

3.3003.3503.3003.325

29252525

3.3073.3083.3083.308

0.890.460.890.68

Fat-corrected annual milk yield (kg/cow/year)

1222

112

1 & 2

4448

8270856173587960

29252525

7967785578557855

0.490.190.340.79

Somatic cell count ('000)

1222

112

1 & 2

4448

137.75204.25190.25197.25

29252525

130.52155.48155.48155.48

0.790.140.300.09

*Kruskal-Wallis test was used because the sample variances were not homogeneous

DISCUSSION

BVD bulk milk survey of DAISY herds

The prevalence of BVDV antibody-positive herds among those on the DAISY herd recording scheme was virtually identical to the prevalence found by Paton and others (1998) in a 1996 survey of 1070 dairy herds in England and Wales. In both studies, around 95 per cent of the herds had evidence of exposure to BVDV (Classes 1, 2 and 3) and 65 per cent of herds had a high level of BVDV antibody (Class 3) in bulk milk (Kossaibati and others 2000).

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MAFFproject code

OD 0339

Bulk tank milk monitoring of BVDV naive herds

The BVD bulk milk survey of DAISY herds was carried out to find herds that were most likely free from BVDV infection, that is, BVDV naive. Based on a single bulk milk antibody ELISA test, a herd was classified as BVDV naive if it had a BVDV antibody level in Class 0 or Class 1. Ideally, to be highly confident that a herd was free from active BVDV infection, only herds in Class 0 should have been selected for the study. However, with only 17 (4.3%) of the 394 DAISY herds in Class 0, this would have left too few herds for the study. Therefore, herds in Class 1 were also considered free from BVDV infection, which increased the potential sample size to 54 herds. Ultimately, 40 farmers were recruited for the follow-up study, which was good when the long-term commitment required by the veterinary surgeons and farmers was considered.

Regular testing of bulk milk for BVDV antibodies was used to determine when a BVDV naive herd became infected with BVDV. If a herd experienced a significant rise in its bulk milk BVDV antibody level, this triggered a warning that the herd might have become infected with BVDV. In the study, a rise in BVDV antibody level was considered significant if it put the herd in Class 2 or Class 3 and it at least doubled the lowest OD ratio recorded in the herd to date. The rise in BVDV antibody level also had to be verified by a second bulk milk test. These criteria were chosen to prevent herds being classed as infected on the basis of natural variation in OD ratios. BVDV antibody levels in bulk milk samples collected only a few weeks apart can vary by as much as 10 to 20 per cent in a herd depending on calving patterns, the number of cows contributing to the sample and their relative milk yields and antibody titres (Pritchard 1998). Eight herds in the study had at least one bulk milk test result in Class 2 but were not classed as potentially infected because the rise in BVDV antibody titre was not sustained. Another herd was deemed uninfected because one bulk milk test result in Class 3 (OD ratio = 0.85) was significantly different from the rest of its test results, which ranged from 0.00 to 0.40. The rises in bulk milk antibody level were also not sustained.

Regular bulk milk antibody testing is a cost-effective and simple means of detecting BVDV infection in a previously BVDV naive herd. However, it is possible for a herd to have a persistently infected cow in the milking herd and to have a low bulk milk antibody level (Drew and others 1999, Sandvik and others 2001). This is probably due to soluble antigen or virus particles in the milk competitively binding BVDV antibody in the milk. Conversely, bulk milk antibodies levels may rise when cows previously exposed to BVDV but no longer actively infected enter the milking herd. As these cows may have been exposed to BVDV on another farm, they may not be indicative of active BVDV in a herd.

Because of cost and the requirement for individual animal testing, the BVDV antigen ELISA was not used to confirm active infection in the suspected BVDV breakdown herds. The study also started too early to take advantage of a newly developed RT-PCR test to detect BVD virus in bulk milk (Drew and others 1999). RT-PCR has been shown to be highly sensitive at detecting persistently infected cows in the milking herd, so it would have been useful to detect herds with persistently infected cows but low bulk milk antibody levels. However, the sensitivity of the test for detecting acutely infected cows, which shed much lower levels of virus than persistently infected animals, is not known.

Incidence of BVDV breakdowns

Two types of incidence rate are reported in the study. The true incidence rate, which is based on herd-years at risk, is used when the population being studied is very dynamic over the time period of interest. It is particularly useful when herds are observed for different periods of time as occurred in this study where herds were monitored for periods ranging between 25 and 33 months. However, true incidence rates are more difficult to interpret than risk rates, which provide a direct estimate of the probability of a herd experiencing the event of interest.

In this study, the risk of a herd experiencing a BVDV breakdown over the course of a year was around 10 to 11 per cent. This is the first time that a systematic study has been done of the rate at which herds become

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MAFFproject code

OD 0339

infected with BVDV in England. In Denmark, the risk of a BVDV naive herd becoming infected with BVDV was estimated at between 34 and 52 per cent per year (Houe 1995). As the prevalence of herds with BVDV antibodies in Denmark was similar to that in the UK at the time, it was expected that the proportion of herds in the study that became infected with BVDV would be close to that in Denmark. This was supported by information from earlier BVD research in England, in which 28 per cent (24/86) of herds with low bulk milk antibody levels had become bulk milk antibody positive (OD>0.3) over the period of a few months (Drew and others 1999). When converted to an annual rate, the incidence of BVDV herd breakdowns was around 40 per cent.

The lower than expected incidence rate of BVDV herd breakdowns may have been due to increased farmer awareness of BVD. At the end of 1996, a BVD vaccine was marketed in the UK for the first time. Articles also appeared in farming journals about the adverse effects of BVD and the eradication schemes being undertaken in the Scandinavian countries. It is interesting to note that the annual incidence rate of BVDV herd breakdowns fell in each of the three years of the study. It is likely that the regular monitoring of their herds for BVDV stimulated farmers to take a more active role in preventing the virus entering their herds. If this was the case, the use of bulk milk tests to monitor endemic infections on dairy farms could be a powerful tool to improve biosecurity on farms (Pritchard 1998).

Source of BVDV infection in the BVDV breakdown herds

The most common source of BVDV infection for the herds in this study was purchased cattle. However, in four of the five herds where purchased cattle were not implicated, no obvious source of BVDV infection was found. In two of the four herds for which no source of infection was identified, there was doubt about whether the milking herd was actively infected with BVDV. The rise in bulk milk antibody level may have been caused by the addition to the milking herd of cows that had been exposed to BVDV in the past but were no longer infected. A third herd may have been infected with BVDV before the study started.

The results of the detailed epidemiological investigations of the BVDV breakdown herds suggested that the rate at which the herds became infected with BVDV was overestimated. In those herds where uninfected cattle with high BVDV antibody titres were bought in and added to the milking herd, a significant rise in bulk milk antibody level was not a good proxy measure of a new viral infection in the herd. However, the additional laboratory tests carried out as part of the epidemiological investigation did help to clarify the situation in these herds.

The study confirmed the importance of purchased cattle as a source of BVDV infection for BVDV naïve herds (Houe 1999, Valle and others 1999) and the necessity to test these animals for BVDV before they join the herd. The testing should also include purchased and hired or shared bulls. In the study, bulls were implicated as a source of BVDV infection in two herds.

Losses in BVDV naive dairy herds that became infected with BVDV

The losses due to various forms of BVDV infection have been summarised by Houe (1999). They include reduced conception rate, abortion, congenital defects, growth retardation after foetal infection, reduced milk production, respiratory disorders, increased levels of other diseases, and death, most commonly from mucosal disease. Most attempts to measure the level of losses in BVDV infected herds have been done on herds with clinical outbreaks of BVD (Duffell and others 1986, Pritchard and others 1989). Therefore, the results are not representative of BVDV infected herds in general and probably overstate the economic effects of the disease in the population as a whole. In this study, the aim was examine the effects of BVDV infection in newly infected herds that were not selected on the basis of clinical outbreaks of BVD but which were more representative of the dairy herd population.

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Projecttitle


MAFFproject code

OD 0339

Because it is costly and difficult to collect data on the reproductive and productive performance of herds, herds in which this information was recorded on a routine basis were selected for the study. In this study, herds on the DAISY dairy information system were used. As the prevalence of exposure to BVDV in these herds was similar to that in the general dairy herd population (Kossaibati and others 1999), they were considered a reasonably representative sample, although it is always likely that farmers who use herd recording schemes will have higher performing herds.

In this study, no statistically significant difference was found between the reproductive performance, disease outcomes, milk yield and somatic cell counts of the BVDV breakdown herds and the herds that remained BVDV naïve. The most likely reason for these results was the small sample size. Based on estimates of the likely incidence of BVDV breakdowns, it was expected that at least half of the 40 herds would become infected with BVDV. In the event, only ten herds met the definition of a BVDV breakdown herd.

When BVDV infection enters a herd, its adverse effects are not always immediately apparent. It may spread slowly through the milking herd and any effects on reproductive performance, milk yield and disease outcomes may be small or transient. This is especially likely if BVDV infection is introduced into the milking herd through an acutely infected cow rather than a persistently infected animal. Significant losses may not be seen until cows in the milking herd give birth to persistently infected calves and these animals enter the milking herd. Therefore, it is important that a study to measure economic losses in newly infected herds has a sufficient follow-up period to allow the full spectrum of disease effects to occur. In retrospect, the follow-up period in this study of two years was too short. In herds that had a BVDV breakdown towards the end of the study, there was virtually no time over which to observe the consequences of the disease. Each breeding cow in a herd also had to go through a full reproductive year before the fertility data for the herd could be calculated reliably. Consequently, only one year’s reproductive performance data and four BVDV breakdown herds were available for analysis.

Although there were no statistically significant differences between the performance of the BVDV breakdown and BVDV naive herds, some results did suggest an adverse effect due to the disease. The abortion rate, per cent of calves born dead and mortality rate were slightly higher in the BVDV breakdown herds. Average annual somatic cell counts were also higher in the BVDV breakdown herds. Niskanen and others (1995) carried out a similar study in Swedish dairy herds. A recent introduction of BVDV was deemed to have occurred in seven (3.3%) of the 213 dairy herds, which they monitored using the bulk milk BVDV antibody ELISA. With a small sample size, they found few statistically significant differences in reproductive and disease outcomes between the newly infected herds (LOHI group) and BVDV naïve herds (LOLO group). The LOHI group received more oestrus-stimulating treatments during service periods and had a higher risk of veterinary-treated cases of mastitis and retained placenta. A poor reproductive performance was more apparent in a third group of herds in their study (HIHI group), which had a uniformly high BVDV antibody level throughout the one-year study.

POSSIBLE FUTURE WORK

No further work on quantifying the losses caused by BVDV is proposed. Since this project was conceived in 1997, a BVDV vaccine has became available in the UK, which has been shown to protect cattle from BVDV and prevent transplacental infection (Brownlie and others 1995). Because the vaccine is expensive, studies which compare the losses between vaccinated and unvaccinated cows on the same farms have been carried out to demonstrate its cost-effectiveness (Curwen 1999). New computer models have also been developed to explore the cost-effectiveness of different options for the control of BVDV on farms (Gunn and others 1998).

When the project started, there was concern about the possibility that the UK might have to follow other EU countries in eradicating BVDV from its national herd. Given the high level of BVDV infection in the UK, there was uncertainty about whether there would be an economic benefit from pursuing the eradication option. In

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MAFFproject code

OD 0339

the future, a cost-benefit analysis of a national eradication programme for BVDV could prove useful to inform government policy in this area.

ACKNOWLEDGEMENTS

We thank the veterinary surgeons and farmers using DAISY who took part in this study and the Veterinary Laboratories Agency Langford for the laboratory analyses. The research was funded by a grant from the Ministry of Agriculture, Fisheries and Food (OD0339).

REFERENCES

BENNETT, R. M. & DONE, J. T. (1986) Control of the bovine pestivirus syndrome in cattle: A case for social cost-benefit analysis? In: Proceedings of the Society of Veterinary Epidemiology and Preventive Medicine, Edinburgh, April 1986, pp.54-65

BENNETT, R. M. & DONE, J. T. (1987) The economics of the bovine pestivirus syndrome at the farm level. In: Proceedings of the Society of Veterinary Epidemiology and Preventive Medicine, Solihull, UK, April 1987, pp.16-25

BROWNLIE, J., CLARKE, M. C. & HOWARD, C. J. (1984) Experimental production of fatal mucosal disease in cattle. Veterinary Record 114, 535-536

BROWNLIE, J., CLARKE, M. C., HOOPER, L. B. & BELL, G. D. (1995) Protection of the bovine fetus from bovine viral diarrhoea virus by means of a new inactivated vaccine. Veterinary Record 137, 58-62

CURWEN, A. (1999) Bovine viral diarrhoea virus (BVDV) infection in cattle herds – control for the future. Cattle Practice 7, 5-9.

DAVID, G. P., CRAWSHAW, T. R., GUNNING, R. F., HIBBERD, R. C., LLOYD, G. M. & MARSH, P. R. (1994) Severe disease in adult dairy cattle in three UK dairy herds associated with BVD virus infection. Veterinary Record 134, 468-472

DREW, T. W., YAPP, F. & PATON, D. J. (1999) The detection of bovine viral diarrhoea virus in bulk milk samples by the use of a single-tube RT-PCR. Veterinary Microbiology 64, 145-154

DONE, J. T., TERLECKI, S., RICHARDSON, C., HARKNESS, J. W., SANDS, J. J., PATTERSON, D. S. P., et al. (1980) Bovine virus diarrhoea-mucosal disease virus: pathogenicity for the fetal calf following maternal infection. Veterinary Record 106, 473-479

DONIS, R. O., CORAPI, W. & DUBOVI, E. (1991) Bovine viral diarrhea virus proteins and their antigenic analyses. Arch. Virol. Suppl. 3, 29-40

DUFFELL, S. J., SHARP, M. W. & BATES, D. (1986) Financial loss resulting from BVD-MD virus infection in a dairy herd. Veterinary Record 118, 38-39

GUNN, G. J., STOTT, A. W. & SCANLAN, S. A. (1998). Estimating the losses associated with bovine viral diarrhoea (BVD) within the Scottish cow-calf herd. In: Proceeding of the 20th World Buiatrics Congress, Sydney, Australia, 2, 1015-1017

HARKNESS, J. W., SANDS, J. J. & RICHARDS, M. S. (1978) Serological studies of mucosal disease virus in England and Wales. Research in Veterinary Science 24, 98-103

HARKNESS, J. W. (1987) The control of bovine virus diarrhoea virus infection. Ann. Rech. Vet. 18, 167-174

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OD 0339

HOUE, H. (1995) Epidemiology of bovine viral diarrhoea virus. Veterinary Clinics of North America: Food Animal Practice 11, 521-547

HOUE, H. (1999) Epidemiological features and economical importance of bovine virus diarrhoea virus (BVDV) infections. Veterinary Microbiology 64, 89-107

HOUE, H., LLOYD, J. W. & BAKER, J. C. (1994) Decision tree analysis of control strategies in Danish dairy herds with outbreaks of mucosal disease. Preventive Veterinary Medicine 21, 133-146

KOSSAIBATI, M. A., CHRISTIANSEN, K. H. & ESSLEMONT, R. J. (2000) Bovine viral diarrhoea virus antibody status of a group of dairy herds in England. Cattle Practice 8, 329-331

LINDBERG, A. (1995) The Swedish control programme on bovine virus diarrhoea – effects on incidence and prevalence after one year in progress. In: Proceedings of the Society of Veterinary Epidemiology and Preventive Medicine – Poster Display and Delegate’s Contact Details, Reading, 132-136.

McCLURKIN, A. W., LITTLEDIKE, E. T., CUTLIP, R. C., FRANK, G. H., CORIA, M. F. & BOLIN, S. R. (1984) Production of cattle immunotolerant to bovine viral diarrhea virus. Canadian Journal of Comparative Medicine 48, 156-161

McGOWAN, M. R., KIRKLAND, P. D., RICHARDS, S. G. & LITTLEJOHNS, I. R. (1993) Increased reproductive losses in cattle infected with bovine pestivirus around the time of insemination. Veterinary Record 133, 39-43

MARTIN, S. W., MEEK, A. H. & WILLEBERG, P. (1987) Veterinary Epidemiology: Principles and Methods. Ames, Iowa State University Press

NISKANEN, R., EMANUELSON, U., SUNDBERG, J., LARRSON, B. & ALENIUS, S. (1995) Effects of infection with bovine virus diarrhoea virus on health and reproductive performance in 213 dairy herds in one county in Sweden. Preventive Veterinary Medicine 23, 229-237

PATON, D. J., CHRISTIANSEN, K. H., ALENIUS, S., CRANWELL, M. P., PRITCHARD, G. C. & DREW, T. W. (1998) Prevalence of antibodies to bovine virus diarrhoea virus and other viruses in bulk tank milk in England and Wales. Veterinary Record 142, 385-391

PRITCHARD, G. C. (1998) Making the best use of bulk milk antibody tests. Cattle Practice 6, 133-137

PRITCHARD, G. C., BORLAND, E. D., WOOD, L. & PRITCHARD, D. G. (1989) Severe disease in a dairy herd associated with acute infection with bovine virus diarrhoea virus, Leptospira hardjo and Coxiella burnetii. Veterinary Record 124, 625-629

SANDVIK, T., LARSEN, I-L. & NYBERG, O. (2001) Influence of milk from cows persistently infected with BVD virus on bulk milk antibody levels. Veterinary Record 148, 82-84

SORENSEN, J. T., ENEVOLDSEN, C. & HOUE, H. (1995) A stochastic model for simulation of the economic consequences of bovine virus diarrhoea virus infection in a dairy herd. Preventive Veterinary Medicine 23, 215-227

STOTT, E. J., THOMAS, L. H., COLLINS, A. P., CROUCH, S., JEBBETT, J., SMITH, G. S., LUTHER, P. D. & CASWELL, R. (1980) A survey of virus infections of the respiratory tract of cattle and their association with disease. Journal of Hygiene Cambridge 85, 257-270

THRUSFIELD, M. (1995) Veterinary Epidemiology. 2nd edition. Oxford, Blackwell Science Limited.

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VALLE, P. S., MARTIN, S. W., TREMBLAY, R. & BATEMAN, K. (1999) Factors associated with being a bovine-virus diarrhoea (BVD) seropositive dairy herd in the More and Romsdal County of Norway. Preventive Veterinary Medicine 40, 165-177.

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