Bovine viral diarrhea virus causes an important production-limiting disease, and the economic impact of this disease has been intensively investigated in dairy1,2 and feedlot cattle.3–5 Bovine viral diarrhea virus has been linked to reproductive losses in beef and dairy herds.6,7 Infectious bovine rhinotracheitis virus is another widely recognized cause of abortion and respiratory tract disease in cattle.6,7 These diseases are considered important differentials when investigating the role of infectious agents in suboptimal productivity in beef herds. However, information on the prevalence of infection and economic impact of these agents in cow-calf herds in North America is limited.8
Serologic testing remains one of the most practical and widely used diagnostic tools for examining the occurrence of several types of common infectious agents, including BVDV and IBR virus. A recent study8 used serologic testing to examine the extent and importance of these diseases in beef cows, but no studies were identified that examined the extent or interpretation of these results in weanling beef calves before mixing at sales and entry into feedlots.
The other factor that could potentially affect serum titers of antibodies against BVDV and IBR virus is the practice of vaccinating calves in the spring during branding and before the cow-calf pairs are moved to summer pasture. Most published literature suggests that passively acquired maternal antibodies expected in most calves < 2 or 3 months of age9 would interfere with the production and persistence of humoral antibody in response to vaccination.10–14 Given these reports, it is unlikely that calves tested in the fall near weaning would have substantial antibody titers as a direct result of vaccination, although this assumption has not been examined in a large field study in beef herds.
In addition to enhancing our understanding of the effect of these agents on cow-calf herd performance, background information about the distribution and extent of serum antibodies at weaning and their potential association with measures of calf health would also be valuable in outbreak investigations. Many investigations of poor productivity are retrospective, especially in extensively managed cow-calf herds. In many instances, before the extent of a problem with excessive calf loss or poor calf performance can be fully recognized, the cattle have been dispersed from the calving area to large pastures. The next practical opportunity to restrain, examine, and test these cattle is at fall processing and weaning. Infectious agents such as IBR virus or BVDV that may have been active in the herd in late gestation or during calving may no longer be present; however, the presence of antibodies in the new calf crop after the decay of passively acquired immunity and given a minimal influence of vaccine-induced titers does suggest the presence of active infection in the herd sometime after the development of calves' immune system in utero.15,16
Many acute infections with BVDV, which can result in high observed antibody titers in weaned calves, are associated with exposure to a PI calf.16,17 These PI calves are important in the maintenance and transmission of BVDV infection.18 A number of techniques have been developed to detect persistent infection in calves, including IHC, antigen capture ELISAs, and PCR tests for ear notches and blood samples.19 However, use of these techniques alone will not allow diagnosis of BVDV in a herd where the PI calf is no longer present because it has died, been sold, or was in transient contact with the herd because of mixing on pasture. The techniques for detecting PI cattle alone are also not sufficient to determine the effects of acute or transient infection in individual cattle or herds, particularly in retrospective investigations.
The first objective of the study reported here was to identify a cohort of weaned calves from herds with high and low perinatal losses and describe the distribution of concentrations of antibodies against IBR virus and BVDV in a sample of calves from each of these groups of herds. The second objective was to examine some of the factors that could be associated with the concentration of those antibodies, including passively acquired maternal antibodies and herd vaccination practices.
Herds with both high and low reported calf losses were recruited to increase the power of the study to meet the primary objective. The study was primarily designed to address the third objective, which was to examine the association between the antibody titers against IBR virus and BVDV as measured in a sample of beef calves at weaning and herd productivity measured as the risk of abortion, stillbirth, calf death before 3 months of age, and calf treatment. The final objective was to examine the association between antibody titers from individual calves, the history of treatment for that calf, and the calf's weaning weight to determine the potential effect of infection on the health and productivity of the individual calf.
Materials and Methods
Selection of herds—The participants were selected for study in the fall of 2002 from a group of 203 cowcalf herds enrolled in a wide ranging study of factors affecting productivity in 3 provinces in western Canada (British Columbia, Alberta, and Saskatchewan). The herds in the larger study of 203 herds were not selected on the basis of productivity or performance criteria. There was no information available on the presence of PI cattle or a history of infectious disease in the 203 herds at the time of enrollment.
The objective of herd selection was to maximize the range of herd calf-loss risk in the final sample. Total proportion of calves lost was determined for each herd on the basis of the sum of reported proportions of abortions, stillbirths, and neonatal deaths for spring 2002. The herds enrolled in this study, typical of many of the commercial and purebred herds in western Canada, calved between January and June, with most herd owners using an established breeding season between May and August. Herds were ranked before fall calf processing on the basis of losses reported by the herd owner. Those in the highest (> 10% total loss) and lowest quartiles (< 6% total loss) were listed in random order. Herd owners from these lists were then approached sequentially until 30 herd owners from each of the high-loss and low-loss groups agreed to participate. Herd owners were paid a small fee per calf sampled to compensate them for their time and to encourage herd owner interest in participating in the study.
Sample collection—Blood samples were collected from a systematic random sample20 of 30 calves from each participating herd in the fall of 2002 after the cow-calf pairs had been removed from summer pasture. Calves at weaning were chosen for study because the interpretation of antibody titers in calves < 4 to 6 months of age can be complicated by the presence of antibodies passively acquired through colostrum absorption.
Ear punch skin biopsy specimens were also collected in the fall of 2002 from these 30 calves by use of a brisket punch that collected a 10-mm circular piece of skin to identify animals that were PI with BVDV. Thirtysix of these herd owners also agreed to testing of all remaining young stock from the herd for determination of BVDV persistent infection status. All samples were fixed in neutral-buffered 10% formalin solution for a minimum of 24 to 48 hours and embedded in paraffin within 1 week of collection.
Laboratory methods—Blood samples were allowed to clot, and the serum was separated and frozen within 48 hours. Serum samples were analyzed for antibodies against IBR virus and BVDV type 1 and 2.
IBR VIRUS ELISA
Infectious bovine rhinotracheitis virus ELISA antigen and tissue control were diluted in buffer and added to alternate rows of 96-well, flat-bottom plates.a Plates were covered by sealing with tape, incubated overnight at 4°C, and washed. Sample serum was diluted to 1:50 in buffer containing 0.2% gelatinb and added to duplicate sets (antigen and tissue culture) of wells. Positive control serum was added at the same dilution to 10 replicate sets of wells. Negative control serum was added as described to 4 replicate sets. After incubation for 1 to 2.5 hours at 37°C, the plates were washed 9 times. Horseradish peroxidase–conjugated protein Gc was diluted 1:5,000 and added before resealing and incubating as before. After the plates were washed 9 times, the horseradish peroxidase–conjugated protein reaction was made visible by addition of orthophenylene diamine substrate,d and the reaction was stopped with 5N HCl. Optical density was read at 490 nm. Antibody titers of test serum samples were reported as a percentage of the positive control serum after both had been adjusted by subtracting the optical density of the negative control serum. The suggested interpretation of ELISA results by the laboratory were as follows: negative, ≤ 8%; suspicious, 9% to 13%; low, 14% to 40%; moderate, 41% to 80%; and high, > 80%.a
BVDV TYPE 1 AND 2 SN ASSAYS
All calf serum samples were tested with a BVDV type 1 SN assay.a Each batch (up to 14 plates with 6 test sera/plate) was made up of a virus (BVDV1/Singer B8232) titration (1 aliquot of the virus/batch was thawed and used, and 1 back-titration of the aliquot/ batch was performed); a positive (calf 72) and negative (fetal calf serum)e control; and the test samples, which were run in duplicate. All samples were then tested in a separate analysis for antibodies against BVDV type 2. Each batch was made up of a virus (BVDV2 B8533) titration and a positive (calf 72) and negative (fetal calf serum)e control, and samples were run in duplicate. The positive control serum (calf 72) was convalescent serum from a calf that was vaccinated with a combination modified-live virus vaccine containing BVDV type 1 and subsequently experimentally infected with a virulent field isolate of BVDV type 2.21 Prior to testing, serum samples were heat inactivated at 56°C for 30 minutes. The first plate of each run used a virus back-titration to ensure that an appropriate virus dilution was used (100 TCID50/100 μL) as well as positive and negative controls. Test sera were diluted via serial 3-fold dilutions and added to the wells. The virus dilution was added to each of the wells, and the plates were incubated at 37°C in CO2 for 2 hours. A cell suspension was prepared by use of embryonic bovine trachea cells in Dulbecco modified Eagle medium with glutamine dipeptidee and 5% irradiated fetal calf sera.e Confluent monolayers of embryonic bovine trachea cells that had been grown for at least 7 days were used. The plates were removed from the incubator, the cells were diluted 1:3, and 50 μL of this solution/well was added on each plate. The plates were sealed with tape and allowed to incubate at 37°C for 7 days. The plates were observed for cytopathic effect by use of an inverted microscope. The interpretation suggested by the laboratory for the SN results for BVDV type 1 were as follows: negative, < 6; suspicious, 6 to 11; low, 12 to 324; moderate, 974 to 8,748; and high, > 8,748.a The laboratory did not provide specific guidelines for interpreting the BVDV type 2 results.
IMMUNOHISTOCHEMICAL ANALYSIS
Ear punch biopsy specimens were examined immunohistochemically by a commercial veterinary laboratory.a Paraffin-embedded skin was serially sectioned, mounted on poly-L-lysine–coated slides, and stained for BVDV with monoclonal antibody 15C5 and an automated IHC technique.22 Diaminobenzidine served as chromogen. Positive control specimens stained concurrently with each batch were tissues from cattle that died from so-called mucosal disease. Serial sections of each block were similarly stained after replacing the monoclonal 15C5 antibody with an irrelevant monoclonal antibody. Evaluators of the IHC results were unaware of the serologic results from the herd. Calves were considered PI if the staining was located in the keratinocytes of the epidermis, in all regions of follicular epithelium, and in the hair bulb and dermal papilla.
Tissue samples collected at postmortem from calves from the same herds in the spring of 2002 were also tested with the same IHC protocol.a The tissue samples tested included skin, heart, lung, ileum, and liver.
Herd management and production data—Additional data were also collected by study-employed veterinarians during on-farm visits before calving, at calving, before breeding, at fall sample collection, and at pregnancy testing to measure a number of individual and herd-level risk factors that may be associated with calf health status. Individual risk factor data included calf birth date, calf sex, date of sample collection, cow age, cow breed, and whether the cow was purchased or born on farm. Herd-level data included whether the cow herd was vaccinated prior to the breeding season in the spring of 2001 and 2002 and whether the calves were vaccinated in the spring of 2002 before being turned out on summer pasture. Vaccine type was also recorded.
All cows and calves were individually identified with at least 1 ear tag. Pregnancy status of individual cows was determined by the herd veterinarian in the fall of 2001 and 2002. Herd risk of nonpregnancy (%) was determined as the number of females found nonpregnant divided by the number of females examined for pregnancy in the fall of the year multiplied by 100. An abortion was defined as either an observed premature calving, judged to have occurred at least 1 month before full term, or an assumed calf loss when a cow was determined to be pregnant but failed to calve. Herd abortion risk was defined as the number of abortions divided by the number of cows retained in the herd after pregnancy testing in which the pregnancy outcome was known.
A stillbirth was defined as a calf that was dead at or within 1 hour of birth or a calf that was found dead, had not been observed alive, and was obviously recently born. Herd risk of stillbirth was calculated as the number of stillbirths expressed as a proportion of the total number of calves born (dead or alive) within 1 month of full-term gestation. A calf death, for the purpose of this analysis, was defined as a calf that died more than 1 hour after birth and before the earlier of 3 months of age or June 30. The herd risk of calf death was the number of calf deaths as a proportion of the total number of calves alive at 1 hour after birth and born before June 30, 2002.
All production data were collected from the herd owners and entered as individual records into a database. Herd inventory was verified during a series of herd visits to ensure that all individual animals were included in the analysis. Detailed calving records at the individual animal level were maintained by the herd owner and included date of birth, cow information, and calf sex, which were used in subsequent analyses. Producers were provided with a standardized treatment book for recording the date of any on-farm treatments, animal identification, class of animal, reason for treatment, type of treatment, outcome, and other notes. The producer was asked to record each treatment occurrence; however, animals reported as treated more than once for the same diagnosis within a 7-day period were classified as having 1 treatment event for the purpose of analysis.
Herd owners were asked to record the identification and date for any known or suspected abortions or calf death losses and to have the animal examined by use of a suggested protocol. Postmortem examinations were to be completed by the herd owner's veterinarian. Laboratory submissions following a standard collection protocol for histologic analysis were encouraged for all postmortem examinations. Multiple tissue samples were examined from all recovered aborted fetuses and dead calves by use of IHC to identify calves PI with BVDV.
Statistical analysis—The differences in herd production variables (abortion, stillbirth, calf death, and nonpregnancy) between high– and low–mortality-risk herds were examined by use of generalized estimating equations with a binomial distribution and logit link function.20,f Similarly, herd vaccination status for BVDV and IBR virus, as well as Campylobacter and Leptospira spp, was examined for potential associations with herd performance variables.
The associations between various animal and herd management factors and antibody titers for each calf were determined by use of mixed models with a random intercept to adjust for clustering by herd.20,g Serologic titers were log transformed before analysis.
The association between serologic status and the occurrence of a previous treatment for each calf was examined by use of a mixed model with a binomial distribution and logit link function.g The association between serologic status and the number of previous treatments for each calf was examined by use of a mixed model with a Poisson distribution and logit link function.g The association between serologic status and fall calf weight was examined by use of a mixed model with a normal distribution.g All individual animal analyses accounted for clustering at the herd level by use of a random intercept.
Calf and cow age, cow breed, vaccination status, and whether the cow was purchased or born on the farm were analyzed for associations with serologic status and calf performance. Any variables that were important confounders (ie, removal of the variable from the model changed the effect estimate for the exposure by ≥ 10%) were also retained in the final model. After establishing a main effect model, biologically reasonable first-order interaction terms were tested if 2 or more variables were retained in the final model. The associations between the prevalence of animals with antibodies of interest at various cutoff titers; herd risk of abortion, stillbirth, and calf death in the 2002 calving season; and risk of nonpregnancy for cows from each herd in the fall of 2002 were examined by use of generalized estimating equations with a binomial distribution and logit link function.f
The adequacy of the models for all endpoints was evaluated by use of plots of residuals that were compared with predicted values. For the models of continuous outcomes, the assumptions of normality and homogeneity of variance were checked starting at the highest level of the hierarchy. For final comparisons, a value of P < 0.05 was considered significant.
Results
Animals and study herds—Blood samples were collected from 1,782 calves from 61 herds in the fall of 2002. A total of 8,159 cows calved in the 61 herds in the spring of 2002. Mean herd size was 163 breeding females at pregnancy testing in 2002 (range, 40 to 486). The calves were a mean ± SD of 227 ± 43 days of age at testing in the fall of 2002. There were more female than male calves tested; 41.1% were steers, 52.7% were heifers, and 6.2% did not have sex reported.
At the time of testing, distributions of the age of the calves' dams were as follows: 15.5% were first-calf heifers bred for their second calf (2.5 years old), 16.3% were 3.5-year-old cows, 55.6% were cows from 4.5 to 10.5 years of age, and 5.6% were > 10.5 years of age. The age was not recorded for 7.0% of the cows. The available information suggested that most cows recorded with missing ages were older than 3 years of age.
Breed type information was also available for the calves' dams; 40.1% were primarily British breed, 47% were primarily continental breeds, 7.5% were mixed breed, and 5.4% did not have breed recorded. Seventy percent of the cows were born on the farm, and 30% were purchased. When body condition score for the cows was measured at pregnancy testing, 8.9% of cows had a body condition score < 5 on the 9-point scale.
Most herd owners vaccinated the cows and heifers with a BVDV and IBR virus vaccine in the 6-month period prior to breeding in 2001. Forty-four percent of the 61 herd owners used an inactivated vaccine in the cow herd before breeding, and 33% used a modified-live vaccine. Twenty-one percent used no vaccine. Eleven (18.0%) herds were also vaccinated against Campylobacter spp with or without Leptospira antigens in the spring of 2001. Vaccination prior to breeding in the spring of 2001 for BVDV and IBR virus was not associated with occurrence of abortion (P = 0.74), stillbirth (P = 0.75), or calf death (P = 0.71) in this group of herds. Similarly, vaccination against Campylobacter spp with or without Leptospira antigens was not associated with abortion (P = 0.12), stillbirth (P = 0.84), or calf death (P = 0.47).
Median total calf loss risk based on individual animal records for all 61 herds was 8.7% (including abortion, stillbirth and calf death; Table 1). For herds with calf loss risk > 8.7%, mean abortion risk was 2.4% (range, 0% to 7.2%); mean stillbirth risk was 4.4% (range, 0% to 11.1%); mean death risk between birth and June 30, 2002, was 8.0% (range, 0% to 18.8%); and mean risk of a calf ever being reported as treated was 13.9%. For herds with calf loss risk < 8.7%, mean abortion risk was 1.3% (range, 0% to 3.7%); mean stillbirth risk was 1.5% (range, 0% to 4.5%); mean death risk between birth and June 30, 2002, was 2.0% (range, 0% to 6.6%); and mean risk of a calf being reported as treated at least once was 16.7%. The herd risks of abortion, stillbirth, calf death, and nonpregnancy were each significantly (P < 0.005) higher in the high–total-mortality-risk group than in the low–total-mortality-risk group.
Risks (%) of variables associated with calf losses and calf treatments in 61 cow-calf beef herds.
| Variable | Mean | Range | Median |
|---|---|---|---|
| Nonpregnancy, 2001 | 7.4 | 0.0–25.7 | 6.5 |
| Abortion | 1.8 | 0.0–7.2 | 1.5 |
| Stillbirth | 2.9 | 0.0–11.1 | 2.2 |
| Death loss (birth to 3 months) | 4.9 | 0.0–18.8 | 3.6 |
| Nonpregnancy, 2002 | 8.6 | 0.0–33.3 | 7.1 |
| Treatment | 15.3 | 0.0–100 | 8.0 |
| Treatment for scours | 7.3 | 0.0–100 | 2.6 |
| Treatment for pneumonia | 2.4 | 0.0–31.3 | 1.0 |
Cows from 58 of these herds were used for pregnancy testing data in the fall of 2002 (mean ± SD herd nonpregnancy risk, 8.6 ± 5.6%). In the 6-month period before breeding in 2002, 51.7% of the 58 herd owners used an inactivated vaccine against BVDV and IBR virus in the cow herd, 25.9% used a modified-live vaccine, and 22.4% did not vaccinate before breeding. Nine (14.8%) of the herds were also vaccinated against Campylobacter spp with or without a Leptospira component in the spring of 2002. This included 7 of the 11 herds in which this vaccine was used in the spring of 2001. There was no association between vaccination in the spring of 2002 against BVDV and IBR virus (P = 0.77) or vaccination against Campylobacter spp with or without a Leptospira component (P = 0.17) and pregnancy status in the fall of 2002.
Twenty-eight percent of herd owners used a modified-live vaccine against BVDV and IBR virus in the calves before the herds were moved to summer pasture in the spring of 2002, and 3% used an inactivated vaccine. There was no association between calf vaccination in the spring of 2002 and calf death (P = 0.29) or cow pregnancy in the fall of 2002 (P = 0.77). Other vaccines used in the calf crop in the spring included clostridial vaccines in all herds, 13 herds vaccinated against Hemophilus somnus, and 5 against Mannhaemia hemolytica. One herd owner administered growth implants in the spring before the cattle were moved to summer pasture.
IBR serology—Five of the 1,770 (0.3%) tested samples had high antibody titers reflected by test results positive at > 80 ELISA units (percentage positive control), 47 (2.7%) had moderate antibody titers (41 to 80 units), 311 (17.6%) had low antibody titers (14 to 40 units), and 1,415 (79.9%) had negative or suspicious antibody titers (< 14 units; Figure 1). Median herd-level prevalence based on this sampling strategy for high concentrations of antibodies against IBR virus (ELISA percentage positive control > 80%) was 0% (range, 0% to 10%); 21 (34.4%) herds had no calves with antibodies against IBR virus (ELISA percentage positive control < 14%).
Distribution of anti-IBR virus titers (sample ELISA optical density U/positive control optical density U × 100%) in serum samples collected from 1,770 weaned calves in the fall of 2002 from low–mortality-risk (< 8.5% total calf loss [black bars]) and high–mortality-risk (≥ 8.5% total calf loss [white bars]) cow-calf beef herds (n = 61).
Citation: American Journal of Veterinary Research 69, 7; 10.2460/ajvr.69.7.916
BVDV type 1 SN antibody—Of the 1,782 samples tested, 781 (43.8%) had SN antibody titers ≥ 256; 410 (23.0%) had SN antibody titers ≥ 1,000; 207 (11.6%) had SN antibody titers ≥ 3,000; and 116 (6.5%) had SN antibody titers ≥ 8,000 (Figure 2) . The prevalence of animals in herds with SN antibody titers > 256 varied from 0% to 100% with a median of 40% (Table 2); 6 of the 61 (9.8%) herds had no calves with a titer > 256.
Distribution of anti-BVDV type 1 virus serum neutralization titers in samples collected from 1,782 weaned calves in the fall of 2002 from low–morality-risk (< 8.5% total calf loss [black bars]) and high–mortality-risk (≥ 8.5% total calf loss [white bars]) cow-calf beef herds (n = 61).
Citation: American Journal of Veterinary Research 69, 7; 10.2460/ajvr.69.7.916
Distribution of herd prevalence risk (No. of seropositive calves/total No. of calves tested) for various anti-BVDV titers in 61 cow-calf beef herds.
| Virus | Titer | |||
|---|---|---|---|---|
| > 256 | > 1,000 | > 3,000 | > 8,000 | |
| BVDV type 1 | ||||
| Minimum | 0.00 | 0.00 | 0.00 | 0.00 |
| Maximum | 1.00 | 0.90 | 0.83 | 0.73 |
| Median | 0.40 | 0.10 | 0.03 | 0.00 |
| 25th percentile | 0.17 | 0.00 | 0.00 | 0.00 |
| 75th percentile | 0.73 | 0.43 | 0.17 | 0.10 |
| Mean | 0.44 | 0.24 | 0.12 | 0.07 |
| SD | 0.32 | 0.28 | 0.18 | 0.13 |
| BVDV type 2 | ||||
| Minimum | 0.00 | 0.00 | 0.00 | 0.00 |
| Maximum | 0.97 | 0.87 | 0.73 | 0.67 |
| Median | 0.17 | 0.03 | 0.00 | 0.00 |
| 25th percentile | 0.03 | 0.00 | 0.00 | 0.00 |
| 75th percentile | 0.47 | 0.14 | 0.07 | 0.03 |
| Mean | 0.28 | 0.14 | 0.09 | 0.07 |
| SD | 0.31 | 0.24 | 0.17 | 0.14 |
BVDV type 2 SN antibody—Of the 1,782 samples collected, 495 (27.8%) had SN antibody titers ≥ 256; 260 (14.6%) had SN antibody titers ≥ 1,000; 157 (8.8%) had SN antibody titers ≥ 3,000; and 122 (6.8%) had SN antibody titers ≥ 8,000 (Figure 3) . Median herd prevalence of animals with SN antibody titers > 256 was 17% (range, 0% to 97%; Table 2); 15 (24.6%) of the herds had no calves with titers > 256.
Distribution of anti-BVDV type 2 virus serum neutralization titers in samples collected from 1,782 weaned calves in the fall of 2002 from low–morality-risk (< 8.5% total calf loss [black bars]) and high–mortality-risk (≥ 8.5% total calf loss [white bars]) cow-calf beef herds (n = 61).
Citation: American Journal of Veterinary Research 69, 7; 10.2460/ajvr.69.7.916
BVDV biopsy and postmortem results—Persistently infected calves were identified through IHC testing of skin punch biopsy specimens; 5,704 biopsies (complete young stock testing in 36 herds and 30 samples/herd in 25 herds) were performed in the 61 herds, and 33 PI calves were found in 14 herds. In the 25 herds in which ≤ 30 calves were biopsied, the resulting prevalence of PI calves was 0.14% (1/717). In the 27 herds with complete young stock testing and no history of a PI calf on the basis of postmortem, the prevalence of PI calves was 0.28% (10/3,550). In the 9 herds with complete young stock testing and a history of a PI calf on the basis of results of the 2002 postmortem examinations, the prevalence of PI calves was 1.53% (22/1,437). The maximum number of PI calves found in 1 herd via biopsy was 9 (6.6% of the calves tested).
Of the 799 calves that were reported to have been aborted, stillborn, or dead within 3 months of birth, 558 (70%) were examined postmortem and tested by use of IHC for BVDV. From this subset of 61 herds, 22 PI cattle were identified on postmortem examination from 13 herds. From the total group of 203 herds, 25 PI cattle were found via postmortem examination in 16 herds (5 were aborted, 1 was stillborn, and 19 died after birth and before June 30), with a maximum of 6 calves in 1 herd. Persistently infected calves were identified in 18 of the 203 herds via results of skin biopsies obtained in fall and postmortem IHC testing.
Association between calf and herd predictors and calf serologic status—Calves born into herds in which the breeding stock and calves were vaccinated with a modified-live virus vaccine had significantly higher concentrations of antibodies against IBR virus than calves from herds that had not been vaccinated (Table 3). Titers of antibodies against BVDV type 1 were also higher in herds in which cows were vaccinated with a modified-live virus vaccine prior to breeding. The IBR virus titers were significantly associated with both BVDV type 1 (Table 4) and II titers (Table 5). Younger calves and calves from cows that were purchased had higher serum antibody titers against BVDV type 2. In addition, BVDV type 1 titers were strongly associated with type 2 titers.
Herd-adjusted unconditional associations between calf, cow, and herd-level risk factors and the log of the ELISA results for serum anti-IBR virus titers in 1,170 beef calves at weaning in 61 herds in 2002.
| Variable | Regression coefficient (β) | 95% CI for β | ||
|---|---|---|---|---|
| Lower | Upper | P value | ||
| Calf age (d) | 0.001 | −0.005 | 0.007 | 0.72 |
| Cow age | ||||
| Bred heifer | −0.014 | −0.063 | 0.035 | 0.59 |
| First-calf heifer | −0.018 | −0.067 | 0.031 | 0.49 |
| Mature cow | Reference category | |||
| > 10 years old | −0.027 | −0.103 | 0.049 | 0.50 |
| Age unknown | −0.004 | −0.078 | 0.070 | 0.91 |
| Cow born on farm | ||||
| Purchased | 0.011 | −0.036 | 0.058 | 0.65 |
| Born on farm | Reference category | |||
| Prebreeding vaccination status (BVDV, IBR) | ||||
| Live | 0.30 | 0.004 | 0.59 | 0.047 |
| Inactivated | 0.12 | −0.16 | 0.40 | 0.40 |
| No vaccine | Reference category | |||
| Calf vaccination (BVDV, IBR) | ||||
| Live vaccine | 0.32 | 0.11 | 0.53 | 0.003 |
| Inactivated vaccine | 0.027 | −0.41 | 0.47 | 0.91 |
| No vaccine | Reference category | |||
Herd-adjusted unconditional associations between calf, cow, and herd-level risk factors and the log of the serum anti-BVDV type 1 antibody titers in 1,782 beef calves at weaning in 61 herds in 2002.
| Variable | Regression coefficient (β) | 95% CI for β | ||
|---|---|---|---|---|
| Lower | Upper | P value | ||
| Calf age (d) | −0.013 | −0.027 | 0.001 | 0.08 |
| Cow age | ||||
| Bred heifer | −0.080 | −0.182 | 0.022 | 0.12 |
| First-calf heifer | −0.015 | −0.119 | 0.089 | 0.78 |
| Mature cow | Reference category | |||
| > 10 years old | 0.127 | −0.034 | 0.288 | 0.12 |
| Age unknown | −0.010 | −0.165 | 0.145 | 0.90 |
| Cow born on farm | ||||
| Purchased | −0.069 | −0.167 | 0.029 | 0.17 |
| Born on farm | Reference category | |||
| Prebreeding vaccination status (BVDV, IBR) | ||||
| Live | 0.53 | 0.13 | 0.93 | 0.01 |
| Inactivated | −0.41 | −1.24 | 0.43 | 0.34 |
| No vaccine | Reference category | |||
| Calf vaccination status (BVDV, IBR) | ||||
| Live | 0.25 | −0.32 | 0.81 | 0.39 |
| Inactivated | −0.03 | −0.57 | 0.50 | 0.90 |
| No vaccine | Reference category | |||
| Log IBR antibody ELISA | 0.63 | 0.53 | 0.72 | < 0.001 |
Herd-adjusted unconditional associations between various individual calf, cow, and herd-level risk factors and the log of the serum anti-BVDV type 2 antibody titers in 1,782 beef calves at weaning in 61 herds in 2002.
| Variable | Regression coefficient (β) | 95% CI for β | ||
|---|---|---|---|---|
| Lower | Upper | P value | ||
| Calf age (d) | −0.018 | −0.032 | −0.004 | 0.01 |
| Cow age | ||||
| Bred heifer | −0.058 | −0.154 | 0.038 | 0.24 |
| First-calf heifer | −0.015 | −0.111 | 0.081 | 0.76 |
| Mature cow | Reference category | |||
| > 10 years old | 0.084 | −0.067 | 0.235 | 0.27 |
| Age unknown | −0.107 | −0.252 | 0.038 | 0.15 |
| Cow born on farm | ||||
| Purchased | −0.099 | −0.191 | −0.007 | 0.04 |
| Born on farm | Reference category | |||
| Prebreeding vaccination status (BVDV, IBR) | ||||
| Live | −0.349 | −0.951 | 0.253 | 0.26 |
| Inactivated | −0.406 | −0.980 | 0.168 | 0.17 |
| No vaccine | Reference category | |||
| Calf vaccination status (BVDV, IBR) | ||||
| Live | 0.16 | −0.30 | 0.62 | 0.50 |
| Inactivated | −0.07 | −1.02 | 0.88 | 0.88 |
| No vaccine | Reference category | |||
| Log IBR antibody ELISA | 0.32 | 0.23 | 0.41 | < 0.001 |
| Log BVDV type 1 SN titer | 0.63 | 0.59 | 0.66 | 0.01 |
Calf serologic status and dam age in PI calves—Of the 1,782 calves from which serum samples were collected, 12 were identified as being PI with BVDV by use of IHC. Because of the relatively small numbers of PI calves in this group, the titers to BVDV and age of the dams were simply described. Of these 12 calves, 7 had a BVDV type 1 antibody titer of < 6. Of the remaining 5 calves, 1 had a titer of 18, 2 had a titer of 54, 1 had a titer of 108, and 1 had a titer of 13,222. For the same 12 calves, 6 had a BVDV type 2 titer of < 6, 1 had a titer of 12, 1 had a titer of 18, 1 had a titer of 36, 1 had a titer of 54, 1 had a titer of 324, and 1 had a titer of 26,244. The PI calf with the extremely high titers for type 1 also had the highest reported titer for type 2. Five of those calves were from heifers, 4 were from 3-year-old cows, 2 were from mature cows, and 1 was from a cow for which the exact age was not recorded.
Association between vaccination in previous breeding season and PI calves in subsequent calf crop—Vaccination of the cows before breeding in 2001 was not associated with the odds of detecting a PI calf in the 2002 calf crop (ORno vaccine to vaccinated, 1.47; 95% CI, 0.37 to 5.81; P = 0.59). Of the 27 herds in which inactivated vaccine was used, 8 (29.6%) herds had at least 1 PI calf; of the 20 herds in which live vaccine was used, 4 (20%) had at least 1 PI calf; and of the 13 herds in which no vaccine was used, 5 had at least 1 PI calf. There was 1 herd with a PI calf that had no record of the type of vaccine used.
Association between either the proportion of calves that were seropositive at weaning or the presence of at least 1 PI calf and herd performance—The proportion of seropositive (IBR ≥ 40 or BVDV type 1 or type 2 ≥ 256, 1,000, 3,000, or 8,000) calves from the fall sample was not associated with dam pregnancy status in 2002 (P = 0.06) or the previous herd risk of abortion (P = 0.11), stillbirth (P = 0.13), or a calf dying before June (P =″ 0.17) following the 2001-2002 breeding season. This finding remained the same when vaccination use in the cows prior to breeding in either 2001 or 2002 was accounted for in the analysis.
There was no association between the presence of at least 1 PI calf detected via examination of postmortem samples and skin biopsy specimens and the herd risk of abortion during the previous calving season (P = 0.59), the risk of stillbirth (P = 0.58), or the herd risk of nonpregnancy immediately following sample collection (P = 0.81). The association between the presence of a PI calf detected either in the fall or from postmortem samples and the herd risk of calf death approached significance (OR, 1.45; 95% CI, 0.99 to 2.14; P = 0.06). However, there was a significant increase in the risk of calf death in herds in which a PI animal was detected through testing of skin biopsy specimens at weaning (OR, 1.58; 95% CI, 1.09 to 2.30; P = 0.02). If the PI calves that died were removed from determination of calf loss, the association decreased and was no longer significant. The data were also reanalyzed considering only the 36 herds in which all calves were biopsied to test for persistent infection status in the fall of 2002, and the resulting conclusions about the associations with reproductive performance and calf survival were identical to the findings from all 61 herds.
Association between calf serologic status at weaning and history of calf treatment—Of the 1,782 calves from which samples were collected, 222 (12.5%) were treated at least once before testing. Individual-calf serologic status was not associated with the calf's history of treatment (Table 6). The odds of treatment of a PI calf, identified by use of skin biopsy specimens, was 6.3 times that of a calf with negative biopsy specimen results, and the number of treatments was a mean of 3.1 times as high in calves with positive results, compared with calves with negative results.
Herd-adjusted association between individual calf serum anti-IBR virus antibody titers, serum anti-BVDV type 1 and 2 antibody titers, persistent infection status for BVDV, odds of ever being treated, and total number of treatments for each calf for 1,782 beef calves in 61 herds.
| Variable | OR | 95% CI for OR | ||
|---|---|---|---|---|
| Lower | Upper | P value | ||
| Ever treated | ||||
| IBR ELISA units > 40 | 0.5 | 0.1 | 3.4 | 0.49 |
| BVDV type 1 titer > 256 | 0.8 | 0.5 | 1.3 | 0.34 |
| BVDV type 2 titer > 256 | 0.7 | 0.4 | 1.2 | 0.24 |
| BVDV-positive biopsy result | 6.3 | 1.3 | 30.3 | 0.02 |
| 95% CI | ||||
| Mean count | Lower | Upper | P value | |
| Total treatments per calf | ||||
| IBR ELISA units > 40 | 0.6 | 0.2 | 1.9 | 0.36 |
| BVDV type 1 titer > 256 | 0.8 | 0.6 | 1.0 | 0.10 |
| BVDV type 2 titer > 256 | 0.7 | 0.5 | 1.1 | 0.09 |
| BVDV-positive biopsy result | 3.1 | 1.0 | 9.4 | 0.04 |
Association between calf and herd-level factors and calf weaning weight—Individual calf weaning weights were available from 676 calves with concurrent blood samples from 26 herds in the fall of 2002; mean weaning weight was 282 ± 53 kg. Other herds either had only group weight data obtained at the time of sale or no fall calf weight information. There was no association between purebred or commercial status and calf weight after accounting for herd effects, sex, cow breed, calf age, dam parity and body condition, twins, persistent infection status, treatment, and vaccination history (P = 0.68). Only one of the herd owners in this study reported administering implants before weaning.
After herd effects, sex, cow breed, calf age, dam parity and body condition, twins, persistent infection status, treatment, and vaccination history were accounted for, fall weights were a mean of 13 kg lower in calves that had titers of antibodies against BVDV type 1 ≥ 1,000 than in calves with titers < 1,000 (Table 7). A similar, but slightly smaller, difference (−9.8 kg; 95% CI, −3.5 to −16.1) was detected if calves with antibody titers ≥ 256 were compared with calves with titers <256. After adjusting for the previously mentioned factors, calves that had anti-BVDV type 2 antibody titers ≥ 256 were 8.6 kg lighter (95% CI, 1.4 to 15.8) and those with anti-BVDV type 2 antibody titers ≥ 1,000 were 15.1 kg lighter (95% CI, 6.3 to 24.0) at fall weighing than those with lower titers. In addition, PI calves weighed 73.5 kg less at weaning than other calves.
Herd-adjusted association between serum anti-BVDV type 1 antibody titers and fall calf weight (kg) accounting for calf sex, calf age at weighing, cow breed and age, whether the calf was a twin, treatment and vaccination history, and body condition score of the cow for 676 beef calves in 26 herds.
| Variable | Regression coefficient (β) | 95% CI for β | ||
|---|---|---|---|---|
| Lower | Upper | P value | ||
| Sex | 0.0001 | |||
| Male | 15.1 | 9.6 | 20.7 | 0.0001 |
| Female | Reference category | |||
| Unknown | −32.7 | −57.2 | −8.2 | 0.01 |
| Breed | 0.0001 | |||
| British | Reference category | |||
| Continental | 15.4 | 5.4 | 25.3 | 0.002 |
| Other breed | 6.1 | −8.3 | 20.4 | 0.40 |
| Unknown breed | −21.3 | −66.8 | 24.1 | 0.37 |
| Calf age (d) | 0.95 | 0.87 | 1.04 | 0.0001 |
| Cow age | 0.0001 | |||
| Bred heifer | −23.3 | −29.9 | −16.7 | 0.0001 |
| First-calf heifer | −11.0 | −17.9 | −4.1 | 0.002 |
| Mature cow | Reference category | |||
| > 10years old | −13.6 | −27.3 | 0.1 | 0.05 |
| Age unknown | 14.0 | −5.6 | 33.6 | 0.16 |
| Twin | −19.1 | −32.1 | −6.1 | 0.004 |
| Cow body condition score < 5 of 9 | −5.6 | −14.5 | 3.3 | 0.22 |
| Calf vaccinated before spring turnout | 0.32 | |||
| No vaccine | Reference category | |||
| Live | −21.9 | −53.1 | 9.3 | 0.17 |
| Inactivated | −18.1 | −59.5 | 23.2 | 0.58 |
| Ever treated | −13.5 | −22.4 | −4.5 | 0.003 |
| BVDV-positive biopsy result | −73.5 | −116 | −30.9 | 0.001 |
| BVDVtype 1 titer > 1,000 | −13.0 | −20.3 | −5.8 | 0.0004 |
Discussion
In this study, we measured the antibody status of beef calves at weaning from herds with a range of reported calf losses during the 2001-2002 production cycle. For most calves, the presence of moderate to high antibody titers at the time of weaning was suggestive of exposure to active infection in the herd sometime after the development of immune competence in utero and before the blood sample was collected in the fall of 2002. There was little evidence of residual passively derived maternal antibodies or vaccine-induced antibodies in the fall samples. The only exception was a small association between IBR virus antibody titers and spring vaccination. There was no association between the proportion of calves with antibodies against any of the diseases examined and pregnancy risk, fetal losses, or calf losses.
However, the risk of calf death was higher in herds in which at least 1 PI calf was detected, compared with herds in which no PI calf was detected. Additional analysis suggested that this effect was primarily associated with deaths in the PI calves, and there was no evidence for a more general effect on herd calf loss from exposure to a PI calf. The PI calves were also more likely to be treated and typically weighed substantially less than their non-PI herdmates at weaning. The most interesting finding was that calves with high titers of antibodies against BVDV (suggesting that they were exposed to a PI calf or had acute BVDV infection sometime late in gestation or in the first months of life) typically weighed less than similar calves that had no evidence of exposure.
The antibody titers were measured in a randomly selected group of calves from both herds with relatively low and high calf losses. The sources of variation in titers to IBR virus and BVDV type 1 and 2 and potential associations with productivity outcomes were examined for each disease.
There was little evidence of recent active IBR virus infection, as reflected by the low prevalence of antibodies in these calves. Less than 3% of the calves had IBR ELISA results suggesting moderate or high antibody titers at the time of sampling. The prevalence of antibodies against IBR virus in calves at weaning was low, compared with a finding of high anti-IBR virus antibody titers in more than 20% of adult cows from similar herds.8 The low prevalence of moderate and high antibody titers in this group of calves suggested that recent active IBR virus infection was uncommon during the spring and summer pasture period preceding sample collection in 2002. However, antibodies against the virus were present in the adult population that were not explained by vaccination history,8 suggesting that there is the long-term potential for natural exposure in these herds and that attention to vaccination programs and biosecurity measures must be maintained.
Exposure to both type 1 and type 2 BVDV was more common than to IBR virus. More than 40% of calves had some evidence of exposure to BVDV type 1, and more than 25% had some evidence of exposure to type 2 viruses, which suggested that type 1 viruses may be more prevalent in this population. Some younger calves and calves from cows that were purchased had higher titers of anti-BVDV type 2 antibodies. The extent of cross-reaction between these 2 types of BVDV was not assessed directly in this study.
Regarding the role of vaccination and passively derived maternal antibody in the observed titers, vaccination at branding may have explained some of the observed IBR virus titers in this group of calves. Calves that had been vaccinated with a modified-live vaccine did have higher titers of antibodies against IBR virus than nonvaccinated calves. Although the association was significant, the potential for spring calfhood vaccination to have a substantial influence on fall IBR virus titers was limited given that the proportion of calves with moderate or high titers was only 3%, that > 28% of herds were composed of vaccinated calves, and that almost half of the calves with moderate to high titers came from nonvaccinated herds.
Titers against BVDV type 1 or 2 were not different between calves that were or were not vaccinated before being moved to pasture in late spring. The serologic response to BVDV vaccination was not surprising given results of other studies10–14 that have examined the effect of high concentrations of passively acquired maternal antibodies on the humoral response to vaccination in young calves. One possible reason for the difference between the IBR virus and BVDV antibody titers may be that the small contribution of vaccination to the IBR virus antibody titers was detectable because natural exposure was apparently relatively infrequent, whereas any residual vaccine titers to BVDV were indistinguishable from the more common field exposures to BVDV during the spring and summer of 2002.
The IBR virus and BVDV type 1 antibody titers were higher in calves from herds in which cows were vaccinated with a modified-live vaccine prior to breeding in 2001 than in those in which cows were not vaccinated. The association with previous-year cow vaccination practices could reflect an increased likelihood of vaccination in herds in which a BVDV or IBR virus problem was suspected. These results were in contrast to those of a previous study23 in which calves < 1 year of age from vaccinated herds were less likely to be BVDV seropositive than calves from unvaccinated herds. Results of the previous study could be explained if PI cattle are less likely to occur in a herd with a good biosecurity and vaccination program. In our study, PI cattle were typically less commonly identified in herds with vaccination programs than in herds without, although the difference was not significant. The power of this comparison was limited by the small number of PI cattle in this study.
The second possible reason for higher antibody titers in calves from cows that were vaccinated was the persistence of increased titers of passively acquired antibodies associated with prebreeding vaccination of the cows the previous year. Given the lack of association between prebreeding vaccine history and antibody titers in the cows at pregnancy testing reported in a 2001 study8 of many of these same herds, this was considered to be an unlikely explanation. If prebreeding vaccination does not increase antibody titers in the cows to a value that can be detected in the fall relative to nonvaccinated cows, it is unlikely that these same cows will have substantially higher concentrations of specific antibodies in their colostrum at calving than nonvaccinated cows. However, the potential presence of passively acquired antibodies in the calves at weaning was evaluated for completeness.
If passively acquired maternal antibodies represented a substantial portion of the titers measured in the fall of 2002, we would expect a strong association between calf age and specific titers as the titers decayed over time. There was no association between calf age and antibody titers for either IBR virus or BVDV type 1. Although there was a small association between calf age and BVDV type 2 antibody titers, further study of the distribution of calf ages and titers relative to other published studies suggested passive titers could explain only a small part of the variation observed in the BVDV type 2 antibody titers. One study12 estimated that it took calves 141 days to become seronegative for anti-BVDV type 1 antibodies and 114 days for anti-BVDV type 2 antibodies. Serum samples were collected from 30 (1.7%) calves that were < 141 days of age and 5 (0.3%) calves in the present study that were < 114 days, of the 1,782 total calves tested for anti-BVDV antibodies. Seventeen of those 30 calves, or < 1% of all calves < 141 days of age, had antibody titers > 256.
Other researchers have reported similar findings regarding the expected decay of passive immunity to BVDV and IBR virus. Kirkpatrick et al11 reported times to seronegative status in 30 dairy calves fed colostrum. Time to seronegative status was 65.1 days for IBR virus, 117.7 days for BVDV type 1, and 94.0 days for BVDV type 2. The half-life of the maternal antibodies in those calves was 12.7 days for IBR virus, 20.5 days for BVDV type 1, and 20.5 days for BVDV type 2. Other researchers also reported a half-life of 21 days for anti-BVDV antibodies in non-PI calves.24,25 Given the short half-life of the passively acquired antibodies and the relatively small number of calves in this group that were young enough at the time of sampling to have moderate or high concentrations of maternal antibodies, the potential of residual passive antibodies to influence the results of these analysis is very limited.
Persistently infected calves were identified by use of IHC in 18 herds. Because some herds were chosen for this study with knowledge of their persistent infection status, it is not appropriate to report the prevalence of herds with PI cattle as a percentage of the 61 herds, as this would overestimate the true herd prevalence. Rather, the study does provide evidence that at least 18 of the 203 herds in the larger study from which these animals were sampled did have at least 1 PI calf.
The term at least is appropriate because the proportion of herds in which a PI calf was detected is likely to be an underestimate of the true prevalence for the following reasons. First, all young stock were tested for persistent infection status in the fall of 2002 in only 36 of the 61 herds. In the other 25 herds, biopsy specimens were collected from 30 animals/herd, and no testing other than postmortem samples was completed in the remaining 142 herds. Second, although > 70% of the calves that died or were aborted in the spring of 2002 in these 61 herds were examined postmortem, some calves that were aborted or died at birth were missed and could have been PI. Therefore, PI calves could have been potentially missed in herds with and without complete herd testing. On the basis of these findings, at least 9% (18/203) of cow-calf herds in western Canada could have at least 1 PI calf. This estimate can be compared with 19% of 52 BVDV-suspect herds and 4% of 72 randomly sampled herds from a previous US survey that also reported at least 1 PI calf.3 In that study, 18,931 calves were screened via single serum samples collected before 4 months of age. The persistent infection status was confirmed by retesting the calves after 6 months of age, and 33 of the 54 that had positive results originally still had positive results. The previous study, did not include postmortem testing of calves that died or were aborted. The percentage of individual calves tested at weaning that were identified as PI within the 61 herds in the present study was 0.6%, compared with 0.3% in the previous US survey of calves < 4 months of age.3
There was no association between antibody titers against IBR virus or BVDV and herd risk of nonpregnancy, abortion, stillbirth, or calf death. There was no association between the presence of a PI calf and the risk of abortion, the risk of stillbirth, or the subsequent risk of nonpregnancy. Given that the presence of a PI calf might have been missed in some herds, there is also a chance that the resulting misclassification could have biased these results toward the null or no observed effect. However, there was an association between the presence of a PI calf and an increase in the herd risk of calf death.
In a previous study,3 herds with PI calves were more likely to have an increased risk of nonpregnancy, compared with herds without PI calves.3 However, herds in the present study were selected to provide a range of calf losses and abortions, whereas more than a third of the herds in the previous study were selected on the basis of a history of reproductive failure. No association with either perinatal or postnatal calf death was detected in that study. It is likely that the present study had greater power to detect an association with calf death and the earlier study had greater power to detect an association with pregnancy risk because of the respective strategies used in herd selection.
The association between the presence of PI calves and the increased risk of calf deaths was also consistent with the finding that PI calves were more likely to be treated for disease and were typically treated more often than non-PI calves. Persistently infected calves were also more likely to be substantially smaller at weaning than non-PI calves. This finding was not surprising given results of previous studies of calves with persistent infection. For example, Taylor et al26 reported that PI calves were a mean of 43 kg lighter than non-PI calves.
The finding that calves with relatively high titers of antibodies against both BVDV type 1 and 2 were lighter at weaning has not been previously documented in cowcalf herds. The difference in weight was estimated after accounting for calf age and sex, whether the calf was a twin, calf vaccination status, cow age and breed type, cow body condition score, pasture condition, history of previous treatment, and calf biopsy result. This finding, which has been anecdotally reported by herd owners with PI calves, could represent an important economic loss to herds with active ongoing BVDV infection.27
Results of the serologic examination reported here suggested that exposure to BVDV types 1 and 2 was much more common in beef calves at weaning than was exposure to IBR virus. Calf vaccination at branding was associated with higher titers of antibodies against IBR virus at weaning, but not to BVDV. Calves from herds in which the cows were vaccinated prior to breeding had higher titers of antibodies against IBR virus and BVDV type 1 at weaning than calves from herds that were not vaccinated. Bovine viral diarrhea virus infection as measured by the presence of PI calves and serologic evidence of infection in weaned calves appeared to have the most substantial impact on cow-calf herd productivity through effects on calf death, the occurrence of calf treatment, and calf weaning weight.
ABBREVIATIONS
| BVDV | Bovine viral diarrhea virus |
| CI | Confidence interval |
| IBR | Infectious bovine rhinotracheitis |
| IHC | Immunohistochemistry |
| OR | Odds ratio |
| PI | Persistently infected |
| SN | Serum neutralization |
Prairie Diagnostic Laboratories, Regina, SK, Canada.
BDH Inc, Toronto, ON, Canada.
Zymed Laboratories, San Francisco, Calif.
IDEXX Laboratories, Westbrook, Me.
Invitrogen Canada Inc, Burlington, ON, Canada.
PROC GENMOD, SAS for Windows, version 8.2, SAS Institute Inc, Cary, NC.
MLwiN, version 2.02, Centre for Multilevel Modelling, London, England.
References
- 1.
Chi J, VanLeeuwen JA, Weersink A, et al. Direct production losses and treatment costs from bovine viral diarrhea virus, bovine leucosis virus, Mycobacterium avium subspecies paratuberculosis, and Neospora caninum. Prev Vet Med 2002;55:137–153.
- 2.
Tiwari A, VanLeeuwen JA, Dohoo IR, et al. Effects of seropositivity for bovine leukemia virus, bovine viral diarrhea virus, Mycobacterium avium subspecies paratuberculosis, and Neospora caninum on culling in dairy cattle in four Canadian provinces. Vet Microbiol 2005;109:147–158.
- 3.↑
Wittum TE, Grotelueschen DM, Brock KV, et al. Persistent bovine viral diarrhea virus infection in US beef herds. Prev Vet Med 2001;49:83–94.
- 4.
O'Connor A, Martin SW, Nagy E, et al. The relationship between the occurrence of undifferentiated bovine respiratory disease and titer changes to bovine coronavirus and bovine viral diarrhea virus in 3 Ontario feedlots. Can J Vet Res 2001;65:137–142.
- 5.
Loneragan GH, Thomson DU, Montgomery DL, et al. Prevalence, outcome, and health consequences associated with persistent infection with bovine viral diarrhea virus in feedlot cattle. J Am Vet Med Assoc 2005;226:595–601.
- 6.
Sanderson MW, Gnad DP. Biosecurity for reproductive diseases. Vet Clin North Am Food Anim Pract 2002;18:79–98.
- 7.
Yamini B, Mullaney TP, Patterson JS, et al. Causes of bovine abortion in the north-central United States: survey of 1618 cases (1983–2001). Bovine Pract 2004;38:59–64.
- 8.↑
Waldner CL. Serological status for N. caninum, bovine viral diarrhea virus, and infectious bovine rhinotracheitis virus at pregnancy testing and reproductive performance in beef herds. Anim Reprod Sci 2005;90:219–242.
- 9.↑
Filteau V, Bouchard E, Fecteau G, et al. Health status and risk factors associated with failure of passive transfer of immunity in newborn beef calves in Quebec. Can Vet J 2003;44:907–913.
- 10.
Ellis J, West K, Cortese V, et al. Effect of maternal antibodies on induction and persistence of vaccine-induced immune responses against bovine viral diarrhea virus type II in young calves. J Am Vet Med Assoc 2001;219:351–356.
- 11.↑
Kirkpatrick J, Fulton RW, Burge LJ, et al. Passively transferred immunity in newborn calves, rate of antibody decay, and effect on subsequent vaccination with modified live vaccine. Bovine Pract 2001;35:47–55.
- 12.↑
Muñoz-Zanzi CA, Thurmond MC, Johnson WO, et al. Predicted ages of dairy calves when colostrum-derived bovine viral diarrhea virus antibodies would no longer offer protection against disease or interfere with vaccination (Erratum published in J Am Vet Med Assoc 2002;221:1281). J Am Vet Med Assoc 2002;221:678–685.
- 13.
Endsley JJ, Roth JA, Ridpath J, et al. Maternal antibody blocks humoral but not T cell responses to BVDV. Biologicals 2003;31:123–125.
- 14.
Fulton RW, Briggs RE, Payton ME, et al. 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 half-life studies and effect on response to vaccination. Vaccine 2004;22:643–649.
- 15.
Grooms DL. Reproductive consequences of infection with bovine viral diarrhea virus. Vet Clin North Am Food Anim Pract 2004;20:5–20.
- 16.
Smith DR, Grotelueschen DM. Biosecurity and biocontainment of bovine viral diarrhea virus. Vet Clin North Am Food Anim Pract 2004;20:131–150.
- 17.
Larson RL, Grotelueschen DM, Brock KV, et al. Bovine viral diarrhea (BVD): review for the beef cattle veterinarians. Bovine Pract 2004;38:93–102.
- 18.↑
Larson RL, Brodersen BW, Grotelueschen DM, et al. Considerations for bovine viral diarrhea (BVD) testing. Bovine Pract 2005;39:96–100.
- 19.↑
Fulton RW, Hessman B, Johnson BJ, et al. Evaluation of diagnostic tests used for detection of bovine viral diarrhea virus and prevalence of subtypes 1a, 1b, and 2a in persistently infected cattle entering a feedlot. J Am Vet Med Assoc 2006;228:578–584.
- 20.↑
Dohoo I, Martin W, Stryhn H. Veterinary epidemiologic research. Charlottetown, PE, Canada: AVC Inc, 2003;502–504.
- 21.↑
Cortese VS, West KH, Hassard LE, et al. Clinical and immunologic responses of vaccinated and unvaccinated calves to infection with a virulent type-II isolate of bovine viral diarrhea virus. J Am Vet Med Assoc 1998;213:1312–1319.
- 22.↑
Haines DM, Clark EG, Dubovi EJ. Monoclonal antibody-based immunohistochemical detection of bovine viral diarrhea virus in formalin-fixed paraffin-embedded tissues. Vet Pathol 1992;29:27–32.
- 23.↑
Paisley L, Wells S, Schmitt BJ. Prevalence of bovine viral diarrhea antibodies in 256 US cow-calf operations: a survey. Theriogenology 1996;46:1313–1323.
- 24.
Brar JS, Johnson DW, Muscoplat CC, et al. Maternal immunity to infectious bovine rhinotracheitis and bovine viral diarrhea viruses: duration and effect on vaccination in young calves. Am J Vet Res 1978;39:241–244.
- 25.
Palfi V, Houe H, Philipsen J. Studies on the decline of bovine virus diarrhoea virus (BVDV) maternal antibodies and detectability of BVDV in persistently infected calves. Acta Vet Scand 1993;34:105–107.
- 26.↑
Taylor LF, Janzen ED, Ellis JA, et al. Performance survival necropsy and virological findings from calves persistently infected with the bovine viral diarrhea virus originating from a single Saskatchewan beef herd. Can Vet J 1997;38:29–37.
- 27.↑
Larson RL, Pierce VL, Grotelueschen DM, et al. Economic evaluation of beef cowherd screening for cattle persistently-infected with bovine viral diarrhea virus. Bovine Pract 2002;36:106–112.
