Effect of constant exposure to cattle persistently infected with bovine viral diarrhea virus on morbidity and mortality rates and performance of feedlot cattle

Daniel L. Grooms Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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Kenny V. Brock Department of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL 36849.

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Steven R. Bolin Department of Pathobiology and Diagnostic Investigation, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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Dale M. Grotelueschen Zoetis, 5 Giralda Farms, Madison, NJ 07940.

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Victor S. Cortese Zoetis, 5 Giralda Farms, Madison, NJ 07940.

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Abstract

Objective—To determine the effects of constant exposure to cattle persistently infected (PI) with bovine viral diarrhea virus (BVDV) on health and performance of feedlot cattle.

Design—3 controlled trials.

Animals—Crossbred feedlot cattle (trial 1, n = 184; trial 2, 138; trial 3, 138).

Procedures—Weaned calves were or were not vaccinated against BVDV at feedlot arrival (trial 1) or 2 (trial 2) or 3 (trial 3) weeks before feedlot arrival. During trial 1, half of the calves were commingled with PI cattle throughout the feeding period. During trial 2, 63 calves were exposed to PI cattle before weaning and all calves were exposed to PI cattle throughout the feeding period. During trial 3, all study calves were exposed to PI cattle throughout the feeding period. Morbidity and mortality rates and average daily gain (ADG) data were analyzed.

Results—During trial 1, calves maintained with PI cattle had a higher morbidity rate regardless of BVDV vaccination than did calves not exposed to PI cattle; however, for calves maintained with PI cattle, the morbidity rate for those vaccinated against BVDV was less than that for those not vaccinated against BVDV. During trial 2, calves exposed to PI cattle before weaning or vaccinated against BVDV had lower morbidity and mortality rates and increased ADG, compared with those for calves not exposed to PI cattle before weaning or vaccinated against BVDV. During trial 3, health and performance did not vary between calves that were and were not vaccinated against BVDV.

Conclusions and Clinical Relevance—Exposure of cattle to BVDV naturally or through vaccination before or at feedlot arrival mitigated the negative effects of constant exposure to PI cattle.

Abstract

Objective—To determine the effects of constant exposure to cattle persistently infected (PI) with bovine viral diarrhea virus (BVDV) on health and performance of feedlot cattle.

Design—3 controlled trials.

Animals—Crossbred feedlot cattle (trial 1, n = 184; trial 2, 138; trial 3, 138).

Procedures—Weaned calves were or were not vaccinated against BVDV at feedlot arrival (trial 1) or 2 (trial 2) or 3 (trial 3) weeks before feedlot arrival. During trial 1, half of the calves were commingled with PI cattle throughout the feeding period. During trial 2, 63 calves were exposed to PI cattle before weaning and all calves were exposed to PI cattle throughout the feeding period. During trial 3, all study calves were exposed to PI cattle throughout the feeding period. Morbidity and mortality rates and average daily gain (ADG) data were analyzed.

Results—During trial 1, calves maintained with PI cattle had a higher morbidity rate regardless of BVDV vaccination than did calves not exposed to PI cattle; however, for calves maintained with PI cattle, the morbidity rate for those vaccinated against BVDV was less than that for those not vaccinated against BVDV. During trial 2, calves exposed to PI cattle before weaning or vaccinated against BVDV had lower morbidity and mortality rates and increased ADG, compared with those for calves not exposed to PI cattle before weaning or vaccinated against BVDV. During trial 3, health and performance did not vary between calves that were and were not vaccinated against BVDV.

Conclusions and Clinical Relevance—Exposure of cattle to BVDV naturally or through vaccination before or at feedlot arrival mitigated the negative effects of constant exposure to PI cattle.

Bovine respiratory disease remains one of the most common causes of morbidity and death as well as economic loss in the beef cattle industry worldwide.1 Regarded as a disease complex, BRD has multiple viral and bacterial etiologies. Additional factors contributing to the pathogenesis of BRD include stress associated with the marketing, shipping, handling, and commingling of cattle; insufficient immunity against respiratory tract pathogens; and adverse environmental conditions. Bovine viral diarrhea virus is an important pathogen involved in the development of BRD2 and is believed to cause profound generalized suppression of nonspecific and specific respiratory tract defense mechanisms, which frequently results in the development of secondary bacterial pneumonia.3 Additionally, BVDV is associated with several other clinical conditions such as diarrhea, bleeding disorders, and undifferentiated fevers that are detrimental to cattle health and performance.4 In the cattle feeding industry, processing programs routinely include vaccines against BVDV to mitigate the negative effects of BVDV infection; however, the efficacy of BVDV vaccination programs is frequently less than optimal because of antigenic variation among BVDV strains, timing of vaccine administration, and immunosuppression that develops secondary to stress as cattle move through marketing channels.

Cattle PI with BVDV (PI cattle) maintain the virus in the cattle population and are the major source of virus exposure for naïve cattle. Epizootiological studies5,6 estimate that < 0.5% of cattle entering beef feedlots are PI with BVDV. The effect that PI cattle have on overall feedlot performance is unclear, and it is necessary to further elucidate the impact of PI cattle on the health and performance of commingled penmates to justify BVDV control programs on commercial cattle operations.

The purpose of the study reported here was to determine the effects of constant exposure to PI cattle and timing (2 or 3 weeks before weaning or at feedlot arrival) of vaccination against BVDV on the health and performance of feedlot cattle. The study was divided into 3 separate trials. The objective for trial 1 was to determine whether vaccination of BVDV-naïve calves against BVDV within 24 hours after arrival at the feedlot would mitigate the negative effects of constant exposure of calves to PI cattle. The objective for trial 2 was to determine whether vaccination of BVDV-naïve calves against BVDV 2 weeks prior to arrival at the feedlot (ie, preconditioning) would mitigate the negative effects of constant exposure of calves to PI cattle. The objective for trial 3 was to determine whether vaccination of BVDV-naïve calves against BVDV 3 weeks prior to arrival at the feedlot would mitigate the negative effects of constant exposure of calves to PI cattle. The hypothesis for each of the trials was that calves vaccinated against BVDV would have better measures of health (decreased morbidity, retreatment, repull, and mortality rates) and performance (increased ADG), compared with those of calves that were not vaccinated against BVDV.

Materials and Methods

All study procedures were approved by the Michigan State University Institutional Animal Care and Use Committee. All cattle were owned by Michigan State University, and all 3 trials were conducted at the Michigan State University Beef Cattle Teaching and Research Center located in East Lansing, Mich.

PI cattle—For all 3 trials, PI (exposure) cattle were obtained from a group of such cattle that was maintained by one of the investigators (DLG). Cattle in that group were PI with various BVDV genotypes and were obtained from commercial farms following confirmation that they were PI with BVDV. Each animal was confirmed to be PI on the basis of serial detection of BVDV in tissue or blood samples obtained at a minimum interval of 3 weeks apart, and the genotype of the infecting virus was determined by real-time PCR assay Exposure cattle were chosen from the group to most closely match the naïve cattle they were to be housed with on the basis of age, body weight, and sex. An attempt was made to include PI cattle that represented both genotypes 1 and 2 in each trial, but this was not a primary selection criteria.

Sample size calculation—For trial 1, the sample size required to detect at least a 10% difference in ADG was calculated by use of the following equation:

article image

where n is the sample size per treatment group, Zα is the standard normal value for the desired 95% confidence level (ie, 1.96), Zβ is the standard normal value required for a power of 80% (ie, −0.84), σ is the a priori estimate of the standard deviation in ADG (0.23 kg [0.5 lb]), μ is the a priori estimate of the mean ADG for feedlot cattle not exposed to cattle PI with BVDV (1.59 kg [3.50 lb]), and μ2 is the a priori estimate of ADG for feedlot cattle continuously exposed to cattle PI with BVDV (1.43 kg [3.15 lb]).7 The sample size was calculated to be a minimum of 35 cattle/treatment group.

For trials 2 and 3, the sample size needed to detect at least a 20% difference in the morbidity rate was calculated by use of the following equation:

article image

where p1 is the a priori estimate of the morbidity rate for feedlot cattle not exposed to cattle PI with BVDV (0.20), p2 is the a priori estimate of the morbidity rate for feedlot cattle continuously exposed to cattle PI with BVDV (0.40), q1 is equivalent to 1 – p1, and q2 is equivalent to 1 – p2.7 The sample size was calculated to be 63 cattle/treatment group.

Effect of vaccination against BVDV within 24 hours after feedlot arrival on morbidity and mortality rates and performance of feedlot cattle that were and were not continuously exposed to PI cattle throughout the feeding period (trial 1)—Trial 1 was conducted between May and December of 2003 and had a 2 × 2 factorial design. Calves were continuously exposed or unexposed to PI cattle, and calves in each exposure group were or were not vaccinated against BVDV within 24 hours after arrival at the feedlot.

Animals, housing, and care

One hundred eighty-four crossbred beef calves (mean weight, 227.27 kg [500 lb]) were purchased from 2 Alabama farms that had been screened for and declared free of PI cattle. Prior to purchase and assembly in Alabama, all calves were confirmed to not be PI with BVDV on the basis of negative results for virus isolation and SNA titers < 1:4 for both genotype 1 and 2 BVDV Calves were stratified on the basis of source (farm 1 or farm 2), sex (male or female), and frame score8 (< 5 or ≥ 6) and were blocked into groups of 4 within each stratum on the basis of weight (< 181.82 kg [< 400 lb], 181.82 to < 227.27 kg [400 to < 500 lb], 227.27 to < 272.73 kg [500 to < 600 lb], or ≥ 272.73 kg [≥ 600 lb]). Calves within each block were randomly allocated to 1 of 4 treatment groups (calves not exposed to PI cattle and not vaccinated against BVDV within 24 hours after feedlot arrival [group 1a; n = 46], calves not exposed to PI cattle and vaccinated against BVDV within 24 hours after feedlot arrival [group 1b; 46], calves continuously exposed to PI cattle and not vaccinated against BVDV within 24 hours after feedlot arrival [group 1c; 46], and calves continuously exposed to PI cattle and vaccinated against BVDV within 24 hours after feedlot arrival [group 1d; 46]) by use of a random number generator.a Then, calves in groups 1a and 1b were loaded onto 1 truck and calves in groups 1c and 1d and 2 calves PI with BVDV (one with genotype 1 BVDV and the other with genotype 2 BVDV) were loaded onto another truck. The calves were transported 1,931 km (1,120 miles) to the research feedlot in Michigan.

Upon arrival at the research feedlot, calves in groups 1a and 1b were unloaded into a pen and calves in groups 1c and 1d were unloaded into another pen that was located 183 m (600 ft) from the pen housing the calves in groups 1a and 1b. The pens were identical in size and consisted of a bedded pack in a 3-sided barn with access to an outdoor concrete run. Biosecurity protocols were implemented to minimize the risk of cross-contamination between the 2 pens. Within 24 hours after arrival at the feedlot, all calves were processed and administered a 7-way clostridial vaccineb that also contained a bacterin against Histophilus somni (5 mL, SC), moxidectinc (0.5 mg/kg [0.23 mg/lb], topically), and a growth implantd that contained 200 mg of progesterone and 20 mg of estradiol (SC in the back of an ear). Additionally, calves in groups 1a and 1c were administered an MLV vaccinee that contained antigens for IBRV, PI3V, and BRSV (2 mL, SC), whereas calves in groups 1b and 1d were administered an MLV vaccinef that contained antigens for IBRV, PI3V, BRSV, and genotype 1 BVDV (2 mL, SC). Calves were fed for 168 days, after which they were marketed and transported directly to slaughter.

Feedlot personnel who were trained in cattle health care monitored the calves daily. These personnel were aware of which pen contained the PI cattle, and this was deemed necessary to ensure that appropriate biosecurity practices were followed. However, the personnel were unaware of which calves had or had not been vaccinated against BVDV. In an effort to reduce potential treatment bias, the feedlot personnel were specifically instructed to be consistent in selecting calves for examination and treatment from both trial pens. Calves that feedlot personnel identified as abnormal were examined and treated in accordance with a standard treatment protocol that was created for the trial. All treatments administered to each calf were recorded. Retreatment was defined as a calf that was re-treated 48 hours after the initial treatment. Repull was defined as a calf that responded to the initial treatment but was treated again at least 7 days after the initial treatment. All calves that died during the trial were submitted to the Michigan State University Diagnostic Center for Population and Animal Health for a complete diagnostic workup.

Sample collection and processing

Arrival at the feedlot was designated as day 0. Each calf was individually weighed on days 1 (during processing), 7, 14, 28, 56, 84, 112, 140, and 168 (just before transport for slaughter). For each measurement, ADG was calculated as the weight gained since processing divided by the number of days on feed in the feedlot.

From each calf, nasal swab specimens and 2 blood samples (one [6 mL] collected in a tube that contained an anticoagulant and another [6 mL] collected in a tube without any additives) collected by jugular venipuncture were obtained on days 1, 7, 14, 28, and 56. Nasal swab specimens were processed as described9 to acquire nasal swab supernate. Blood samples that were collected in tubes that contained an anticoagulant were processed as described9 to acquire the buffy coat fractions. Blood samples that were collected in tubes that did not contain any additives were centrifuged at 1,500 × g for 10 minutes to obtain serum.

Nasal swab supernate, buffy coat, and serum samples were analyzed for the presence of BVDV by means of an immunoperoxidase monolayer assay as described.9 Additionally, SNA titers against BVDV genotypes 1 and 2 were determined by use of serum neutralization assays as described9 for serum samples obtained on days 1, 28, and 168. The reference strains of BVDV used for the serum neutralization assays were Singer (genotype 1a) and 125C (genotype 2a).

Effect of vaccination against BVDV 2 weeks before feedlot arrival on morbidity and mortality rates and performance of feedlot cattle that were and were not exposed to PI cattle before weaning and were continuously exposed to PI cattle throughout the feeding period (trial 2)—Trial 2 was conducted between June and September of 2008 and was originally designed as a controlled trial in which BVDV-naïve calves would be systematically vaccinated against BVDV or administered a sham inoculation of sterile water 2 weeks before weaning, after which all calves would be commingled in a pen with 4 PI calves. Unfortunately, the identification of PI calves in the population of supposedly BVDV-naïve calves purchased for the trial necessitated modifications to the trial design. As a result, the hypothesis was modified to calves vaccinated against BVDV 2 weeks before weaning and continuously exposed to PI cattle after weaning would have better measures of health and performance, compared with those for calves not vaccinated against BVDV 2 weeks before weaning, regardless of exposure to PI cattle before weaning. Also, instead of 2 treatment groups (calves that were and were not vaccinated against BVDV 2 weeks before weaning), 4 treatment groups were defined (calves exposed to PI cattle prior to weaning and vaccinated against BVDV 2 weeks before weaning [group 2a], calves exposed to PI cattle prior to weaning and not vaccinated against BVDV 2 weeks before weaning [group 2b], calves not exposed to PI cattle prior to weaning and vaccinated against BVDV 2 weeks before weaning [group 2c], and calves not exposed to PI cattle prior to weaning and not vaccinated against BVDV 2 weeks before weaning [group 2d]).

Animals, housing, and care

Unweaned crossbred beef calves (n = 142; mean weight, 227.27 kg) that had not been vaccinated against BVDV were purchased from a single farm in Virginia. The cows and calves on this farm were divided among 5 management groups that were housed in separate locations. These management groups had been established primarily on the basis of parity (primiparous and multiparous cows), expected calving dates (early calving group and late calving group), and breed (Angus and Crossbred). Each management group had been established the preceding fall after calves were weaned and cows were examined for pregnancy. The management groups ranged in size from 26 to 40 cows.

From each calf prior to trial initiation, an ear notch specimen for real-time PCR assay to detect the presence of BVDV RNA and a blood sample (6 mL) for serum neutralization assay to determine SNA titers against BVDV genotypes 1 and 2 were obtained. Results of real-time PCR assays performed on pooled ear notch specimens (10 ear notch specimens/pool) were negative, which suggested that none of the calves were PI with BVDV; however, evaluation of SNA titers against BVDV for individual calves suggested that some calves had been exposed to BVDV. Results of subsequent testing of individual calves by means of virus isolation on serum samples revealed that 2 of the 5 management groups contained PI calves (one affected management group contained 1 PI calf, and the other affected management group contained 3 PI calves), and the 4 PI calves were all infected with genotype 1b.

Two weeks before weaning, half of the calves in each of the 5 management groups were administered 2 mL of an MLV vaccineg that contained antigens for IBRV, PI3V, BRSV, and BVDV genotypes 1 and 2 IM and the other half were administered 2 mL of sterile water IM. Within each management group, calves were assigned to a vaccination group on the basis of a random number list generated with commercially available software.a Following treatment group allocation, there were 37 calves in group 2a, 30 calves in group 2b, 37 calves in group 2c, and 38 calves in group 2d.

At weaning, the calves were transported to the research feedlot in Michigan, where they were housed in a single pen. Upon arrival, 4 calves PI with genotype 1b BVDV were introduced into the pen. Because the 4 calves PI with genotype 1b BVDV from the source farm were not removed from the trial population, the pen contained 8 calves PI with genotype 1b BVDV and 138 calves not PI with BVDV (group 2a, n = 37; group 2b, 26; group 2c, 37; group 2d, 38).

Twenty-four hours after arrival at the feedlot, all calves were processed and administered a 7-way clostridial vaccineb that also contained a bacterin against H somni (5 mL, SC); a Mannheimia haemolytica bacterin and toxoidh (2 mL, SC); an MLV vaccineg that contained antigens for IBRV, PI3V, BRSV, and BVDV genotypes 1 and 2 (2 mL, IM); doramectini (0.2 mg/kg [0.09 mg/lb], SC); and a growth implantd that contained 200 mg of progesterone and 20 mg of estradiol (SC in the back of an ear). Calves were fed for a period of 84 days, after which they were marketed and transported directly to slaughter.

Feedlot personnel who were trained in cattle health care monitored the calves daily and administered treatments to morbid calves as described for trial 1. Throughout the observation period, feedlot personnel were unaware of the treatment group to which the calves were assigned.

Sample collection and processing

As in trial 1, arrival at the feedlot was designated as day 0. From each calf, an ear notch specimen for detection of BVDV RNA by real-time PCR assay was obtained on day −30 and a blood sample (6 mL) for detection of SNA titers against BVDV genotypes 1 and 2 by serum neutralization assays was obtained on days −30 and 1 (during processing). Additionally, each calf was individually weighed on days 1, 28, 56, and 84 (just prior to transport for slaughter) for calculation of ADG. Nasal swab specimens were obtained on days 6, 8, 14, and 18 for BVDV virus isolation.

Ear notch specimens were processed and screened for the presence of BVDV RNA by use of a real-time PCR assay as described.10 Initially, a real-time PCR assay was performed on pooled specimens (10 ear notch specimens/pool). For pools that yielded positive results for BVDV RNA, the individual ear notch specimens that comprised those pools were evaluated for the presence of BVDV antigen by use of a fluorescent antibody test as described.10 Serum was obtained from clotted blood samples, and serum neutralization assays and virus isolation on nasal swab specimens were performed as described for trial 1.

Effect of vaccination against BVDV 3 weeks before feedlot arrival on morbidity and mortality rates and performance of feedlot cattle that were continuously exposed to PI cattle throughout the feeding period (trial 3)—Trial 3 was conducted between October 2009 and April 2010 and was designed as a randomized clinical trial. Calves were or were not vaccinated against BVDV 3 weeks before weaning. At weaning, the calves were transported to the research feedlot where they were continuously commingled in a pen with 2 PI cattle.

Animals, housing, and care

Unweaned crossbred beef calves (n = 138; mean weight, 227.27 kg) that had not been vaccinated against BVDV were purchased and assembled from 2 farms in Michigan. Prior to purchase, all calves were confirmed to not be PI with BVDV on the basis of negative results for BVDV RNA as determined by real-time PCR assay performed on pooled ear notch specimens (10 ear notches/pool). Calves were stratified by farm (1 or 2) and age into 2 blocks of equal size (69 calves/block), and then calves in each block were randomly allocated by means of a random number list generated with commercially available softwarea to 1 of 2 treatment groups (calves vaccinated against BVDV [group 3a; n = 67] or calves administered a sham inoculation of sterile water [group 3b; 71]). Three weeks before weaning, calves in group 3a were vaccinated with an MLV vaccinef that contained antigens for IBRV, PI3V, BRSV, and BVDV genotypes 1 and 2 (2 mL, SC) and calves in group 3b were administered a sham inoculation of sterile water (2 mL, SC). At weaning, all calves were transported to the research feedlot, where they were commingled in a single pen with 2 calves PI with genotype 2 BVDV.

Twenty-four hours after arrival at the feedlot, all calves were processed and administered a 7-way clostridial vaccineb that also contained a bacterin against H somni (5 mL, SC); a M haemolytica bacterin and toxoidh (2 mL, SC); an MLV vaccineg that contained antigens for IBRV, PI3V, BRSV, and BVDV genotypes 1 and 2 (2 mL, IM); doramectini (0.2 mg/kg, SC); and a growth implantd that contained 200 mg progesterone and 20 mg estradiol (SC in the back of an ear). Calves were fed for 168 days, after which they were marketed and transported directly to slaughter.

Feedlot personnel who were trained in cattle health care monitored the calves daily and administered treatments to morbid calves as described for trial 1. Throughout the observation period, feedlot personnel were unaware of the treatment group to which the calves were assigned.

Sample collection and processing

As in the other 2 trials, arrival at the feedlot was designated as day 0. From each calf, an ear notch specimen for detection of BVDV RNA by real-time PCR assay was obtained on day −30 and a blood sample (6 mL) for detection of SNA titers against BVDV genotypes 1 and 2 by serum neutralization assays was obtained on days −30 and 1 (during processing). Additionally, each calf was individually weighed on days 1, 28, 56, 84, 112, 140, and 168 (just prior to transport for slaughter) for calculation of ADG. Ear notch specimens and blood samples were processed as described for trial 2.

Statistical analysis—The outcomes of interest for trial 1 were ADG and morbidity, retreatment, repull, and mortality rates. Plots of standardized residuals for each continuous outcome were visually examined to verify that model assumptions were met. Descriptive data for each outcome of interest were summarized for each treatment group; ADG, a continuous variable, was reported as the mean (SD), and binary outcomes such as morbidity, retreatment, repull, and mortality were reported as incidence rates for the feeding period.

A mixed general linear model was used to evaluate the association of ADG with exposure to PI cattle and vaccination against BVDV within 24 hours after feedlot arrival. Random effects included in the model were block (1 to 46) to account for clustering of calves within strata before treatment group assignment and day (1, 28, 56, 84, 112, 140, or 168) to account for repeated measurement of ADG within individual calves. A compound symmetry variance-covariance structure was used to model the effect of block, and a first-order autoregressive variance-covariance structure was used to model the effect of day. Treatment group (1a, 1b, 1c, and 1d) was included in the model as a fixed effect and accounted for the interaction between exposure to PI cattle and BVDV vaccination (ie, the 2 × 2 factorial design). Other biologically plausible independent variables assessed as fixed effects in the model included weight on day 1, morbidity status (yes or no), and the interaction between treatment group and day. Post hoc comparisons between treatment groups were performed with the Tukey method.

The respective associations of morbidity, retreatment, repull, and mortality rate with exposure to PI cattle and vaccination against BVDV within 24 hours after feedlot arrival were assessed by use of mixed generalized linear models with a logit link to account for the binary nature of the outcomes. Block was included in each model as a random effect to account for clustering of calves within strata before treatment group assignment by use of a semirobust variance estimator.11 Treatment group was included in the models as a fixed effect and accounted for the interaction between exposure to PI cattle and BVDV vaccination. Other independent variables assessed as fixed effects included weight on day 1 and morbidity status. For each respective model, risk ratios and the accompanying 95% CIs were calculated.

The PI calves from the herd of origin were not included in the analysis for trial 2. The outcomes of interest for trial 2 were calf weight, ADG, and morbidity, retreatment, repull, and mortality rates. Plots of standardized residuals for continuous outcomes were visually examined to verify that model assumptions were met. Descriptive data for each outcome of interest were summarized for each treatment group; continuous variables such as calf weight and ADG were reported as the mean (SD), and binary outcomes such as morbidity, retreatment, repull, and mortality were reported as incidence rates for the feeding period.

Mixed general linear models were used to evaluate the respective associations of calf weight and ADG with vaccination against BVDV and exposure to BVDV before weaning. Calf identification was included in the models as a random effect to account for repeated measures within each calf. Various variance-covariance structures were evaluated to determine which structure provided the best fit for the data, and the structure that minimized the value of the Bayesian information criteria (heterogeneous autoregressive type 1) was used for all subsequent modeling. Fixed effects included in the models were BVDV vaccination (yes or no), exposure to PI cattle before weaning (yes or no), and day (1, 28, 56, or 84). Other independent variables assessed as fixed effects included sex (male or female), calf weight on day 1, and all possible 2-way and 3-way interactions among the fixed effects. Treatment group (2a, 2b, 2c, or 2d) was not included as a fixed effect in the models because it accounted for the interaction between BVDV vaccination and exposure to PI cattle before weaning and we wanted to assess BVDV vaccination separately from exposure to PI cattle before weaning.

The respective associations of morbidity, retreatment, repull, and mortality rates with BVDV vaccination and exposure to PI cattle before weaning were evaluated by the use of mixed generalized linear models with a logit link to account for the binary nature of the outcomes. Source-farm management group was included in each model as a random effect. Fixed effects included in each model included BVDV vaccination, exposure to PI cattle before weaning, and the interaction between BVDV vaccination and exposure to PI cattle before weaning. Other independent variables evaluated as fixed effects included sex and calf weight on day 1. For both the mixed general linear models and mixed generalized linear models, post hoc comparisons between BVDV vaccination status and exposure to PI cattle before weaning (ie, treatment groups) were made with the Tukey method.

The outcomes of interest for trial 3 were calf weight, ADG, and morbidity, retreatment, repull, and mortality rates. Analyses for each outcome were similar to those described for trial 2, except exposure to PI cattle before weaning did not need to be evaluated.

All analyses were performed with statistical software.j,k For all analyses, values of P < 0.05 were considered significant.

Results

Trial 1—During trial 1, BRD was the only adverse health event reported and 2 calves died (one from group 1b and the other from group 1d) because of respiratory disease. The morbidity, retreatment, and repull incidence rates and the accompanying risk ratios were summarized on the basis of treatment group, exposure to PI cattle, and vaccination against BVDV (Table 1). Calves continuously exposed to PI cattle during the feeding period (groups 1c and 1d) were twice as likely to be treated for respiratory disease at least once as were calves not exposed to PI cattle (risk ratio, 2.04; 95% CI, 1.35 to 3.09). However, the risk of being treated for BRD at least once during the feeding period did not differ significantly between calves that were (groups 1b and 1d) and were not (groups 1a and 1c) vaccinated against BVDV. Calves that were affected with BRD and exposed to PI cattle were 5.7 times (95% CI, 1.62 to 19.81) as likely to require retreatment as were calves that were affected with BRD and not exposed to PI cattle. Calves that were affected with BRD and vaccinated against BVDV were 57% less likely (risk ratio, 0.43; 95% CI, 0.17 to 1.06) to require retreatment than were calves affected with BRD that were not vaccinated against BVDV, although this difference did not quite reach significance (P = 0.067). The repull rate did not vary significantly among treatment groups, between calves exposed and not exposed to PI cattle, or between calves that were and were not vaccinated against BVDV.

Table 1—

Morbidity, retreatment, and repull rates and risk ratios for 184 weaned crossbred beef calves that were or were not vaccinated against BVDV within 24 hours after feedlot arrival and were or were not continuously exposed to cattle PI with BVDV (PI cattle) during a 168-day feeding period (trial 1).

OutcomeVariableIncidence rate (%)Risk ratio (95% CI)P value
MorbidityTreatment group   
  1a30.431.56 (0.75–3.23)0.236
  1b19.57Referent
  1c63.043.22 (1.60–6.48)< 0.001
  1d39.132.00 (1.13–5.53)0.017
 Exposure to PI cattle   
  No (groups 1a and 1b)25.00Referent
  Yes (groups 1c and 1d)51.092.04 (1.35–3.09)< 0.001
 Vaccinated against BVDV   
  No (groups 1a and 1c)41.30Referent
  Yes (groups 1b and 1d)34.780.84 (0.58–1.21)0.358
RetreatmentTreatment group   
  1a4.352.00 (0.18–22.00)0.571
  1b2.17Referent
  1c28.2613.00 (1.66–101.82)0.015
  1d8.704.00 (0.44–36.73)0.220
 Exposure to PI cattle   
  No (groups 1a and 1b)3.26Referent
  Yes (groups 1c and 1d)18.485.67 (1.62–19.81)0.007
 Vaccinated against BVDV   
  No (groups 1a and 1c)15.22Referent
  Yes (groups 1b and 1d)6.520.43 (0.17–1.06)0.067
RepullTreatment group   
  1a2.171.00 (0.06–16.57)1.00
  1b2.17Referent
  1c10.875.00 (0.58–43.21)0.144
  1d6.523.00 (0.31–29.25)0.344
 Exposure to PI cattle   
  No (groups 1a and 1b)2.17Referent
  Yes (groups 1c and 1d)8.704.00 (0.80–19.92)0.091
 Vaccinated against BVDV   
  No (groups 1a and 1c)6.52Referent
  Yes (groups 1b and 1d)4.350.67 (0.21–2.11)0.491

Calves were randomly allocated to 1 of 4 treatment groups (calves not exposed to PI cattle and not vaccinated against BVDV within 24 hours after feedlot arrival [group 1a; n = 46], calves not exposed to PI cattle and vaccinated against BVDV within 24 hours after feedlot arrival [group 1b; 46], calves continuously exposed to PI cattle and not vaccinated against BVDV within 24 hours after feedlot arrival [group 1c; 46], and calves continuously exposed to PI cattle and vaccinated against BVDV within 24 hours after feedlot arrival [group 1d; 46]). Morbidity was defined as calves that were treated for BRD at least once. Retreatment was defined as calves that were re-treated for BRD 48 hours after the initial treatment. Repull was defined as calves that responded to the initial treatment but were re-treated for BRD at least 7 days after the initial treatment.

— = Not applicable.

The mean (SD) weight and ADG for each treatment group throughout trial 1 were summarized (Table 2). At initiation of the study, the mean calf weight did not differ significantly among the treatment groups. The ADG for calves not exposed to PI cattle (groups 1a and 1b) was significantly greater than that for calves exposed to PI cattle (groups 1c and 1d) on days 14 and 28; however, the ADG did not differ significantly among the treatment groups for any of the subsequent observations. The ADG on day 168 (just before transport for slaughter) was not associated with treatment group or calf weight on day 1.

Table 2—

Mean (SD) weight and ADG for the calves of trial 1 on days 1 (processing), 7, 14, 28, 56, 84, 112, 140, and 168 (just before transport for slaughter).

  Treatment group
VariableDay1a1b1c1d
Weight (kg)1243.68 (32.92)244.45 (31.79)244.32 (33.22)243.51 (30.79)
 7258.48 (35.11)259.39 (33.08)259.11 (35.62)256.72 (36.46)
 14270.04 (36.47)272.02 (33.19)267.02 (36.28)265.95 (38.05)
 28291.96 (36.89)293.46 (36.41)287.73 (36.28)286.66 (39.42)
 56333.89 (40.70)332.43 (38.40)328.58 (39.27)327.61 (43.94)
 84371.98 (40.41)370.63 (39.48)368.26 (39.96)367.81 (45.51)
 112416.32 (43.13)414.68 (40.89)414.33 (44.77)410.91 (49.58)
 140456.34 (45.45)456.82 (43.84)456.98 (46.10)449.29 (49.43)
 168483.76 (79.36)492.02 (45.90)494.13 (48.71)486.98 (51.38)
ADG (kg)72.11 (0.99)a2.13 (0.82)a2.11 (0.83)a1.89 (0.76)b
 141.88 (0.68)a1.98 (0.60)a1.62 (0.71)b1.60 (0.69)b
 281.72 (0.36)a1.75 (0.35)a1.55 (0.37)b1.54 (0.40)b
 561.61 (0.24)1.57 (0.22)1.50 (0.28)1.50 (0.29)
 841.53 (0.18)1.50 (0.18)1.48 (0.23)1.48 (0.23)
 1121.54 (0.18)1.52 (0.18)1.52 (0.24)1.49 (0.21)
 1401.52 (0.18)1.52 (0.18)1.52 (0.22)1.47 (0.19)
 1681.43 (0.42)1.47 (0.17)1.49 (0.21)1.45 (0.20)

Within a variable and day, values with different superscript letters differ significantly (P < 0.05).

Arrival at the feedlot was designated as day 0. Average daily gain was calculated as the amount of weight gained since processing (day 1) divided by the days on feed at that measurement.

See Table 1 for remainder of key.

Bovine viral diarrhea virus was isolated from both PI calves at all sample collections. For the calves not exposed to PI cattle (groups 1a and 1b), BVDV was not isolated from any sample (nasal swab supernatant, buffy coat, or serum) at any collection. For the calves exposed to PI cattle (groups 1c and 1d), BVDV was isolated from serum and buffy coat samples of all calves on day 7; however, BVDV was not isolated in any samples obtained from those calves during subsequent collections.

The geometric mean (SD) SNA titers against BVDV genotypes 1 and 2 on days 1, 28, and 168 by treatment group were summarized (Table 3). For the calves of group 1a, the mean SNA titers against BVDV genotypes 1 and 2 did not change significantly during the feeding period, whereas for calves in each of the other 3 treatment groups, the mean SNA titers against both BVDV genotypes increased significantly between days 1 and 28 and between days 28 and 168. These findings, along with those for BVDV isolation, suggested that the biosecurity practices implemented at the feedlot were successful in keeping BVDV contamination confined to the pen that contained groups 1c and 1d and the 2 PI calves.

Table 3—

Geometric mean (SD) SNA titers against BVDV genotypes 1 and 2 for the calves of trial 1 on days 1, 28, and 168.

  Treatment group
GenotypeDay1a1b1c1d
110.5 (1.5)a2.1 (2.2)a*2.3 (2.5)b*2.5 (2.0)b*
 280.4 (1.6)a3.8 (2.0)b6.6 (2.4)c6.5 (2.5)c
 1680.2 (1.3)a5.1 (1.8)b8.9 (0.9)c8.9 (0.8)c
210.8 (1.8)a1.9 (2.9)a*2.5 (2.6)b*3.0 (2.7)b*
 281.3 (2.3)a2.9 (2.7)b7.1 (2.7)c6.6 (2.9)c
 1681.2 (1.3)a5.1 (2.5)b8.7 (1.8)c9.1 (1.4)c

Within a genotype and day, values with different letters differ significantly (P < 0.05).

Within a genotype and treatment group, values with different symbols differ significantly (P < 0.05).

A logarithmic (log2) transformation was applied to SNA titers to normalize the distribution of the data for analysis.

See Table 1 for remainder of key.

Trial 2—During the trial period, 3 calves from group 2b died or were euthanized (2 because of cellulitis and 1 because of a vertebral abscess and fracture). The morbidity, retreatment, and repull rates were summarized (Table 4). Morbidity rate was not associated with exposure to PI cattle prior to weaning (P = 0.052) or vaccination against BVDV 2 weeks before weaning (P = 0.580). Retreatment rate was not associated with exposure to PI cattle prior to weaning (P = 0.181) or vaccination against BVDV 2 weeks before weaning (P = 0.065). Although the association did not quite reach significance, calves vaccinated against BVDV 2 weeks before weaning were 75% less likely to be re-treated than were calves not vaccinated against BVDV 2 weeks before weaning (risk ratio, 0.25; 95% CI, 0.06 to 1.09). Repull rate was not associated with exposure to PI cattle prior to weaning (P = 0.784) or vaccination against BVDV 2 weeks before weaning (P = 0.813).

Table 4—

Morbidity, retreatment, and repull rates and risk ratios for 138 crossbred beef calves that were or were not exposed to PI cattle before weaning and were or were not vaccinated against BVDV 2 weeks prior to weaning and then commingled with PI cattle for an 84-day feeding period (trial 2).

OutcomeVariableIncidence rate (%)Risk ratio (95% CI)P value
MorbidityTreatment group   
  2a43.24Referent
  2b42.310.98 (0.55–1.75)0.941
  2c56.761.31 (0.83–2.09)0.251
  2d63.161.46 (0.94–2.27)0.093
 Exposure to PI cattle before weaning   
  No (groups 2c and 2d)60.00Referent
  Yes (groups 2a and 2b)42.850.714 (0.51–1.00)0.052
 Vaccinated against BVDV 2 wk before weaning   
  No (groups 2b and 2d)54.86Referent
  Yes (groups 2a and 2c)50.000.914 (0.60–1.70)0.580
RetreatmentTreatment group   
  2a6.25Referent
  2b9.101.45 (0.10–20.87)0.780
  2c4.760.76 (0.05–11.27)0.843
  2d33.335.33 (0.074–38.64)0.100
 Exposure to PI cattle before weaning   
  No (groups 2c and 2d)20.00Referent
  Yes (groups 2a and 2b)7.400.37 (0.09–1.59)0.181
 Vaccinated against BVDV 2 wk before weaning   
  No (groups 2b and 2d)25.71Referent
  Yes (groups 2a and 2c)5.410.25 (0.06–1.09)0.065
RepullTreatment group   
  2a6.25Referent
  2b9.101.45 (0.10–20.87)0.780
  2c14.292.13 (0.24–18.73)0.497
  2d12.501.89 (0.21–16.72)0.568
 Exposure to PI cattle before weaning   
  No (groups 2c and 2d)13.33Referent
  Yes (groups 2a and 2b)7.400.83 (0.23–3.06)0.784
 Vaccinated against BVDV 2 wk before weaning   
  No (groups 2b and 2d)11.42Referent
  Yes (groups 2a and 2c)10.810.85 (0.23–3.17)0.813

Calves were purchased from a single farm that had cows and calves separated into 5 management groups, 2 of which contained calves PI with BVDV. Within each management group, half the calves were vaccinated against BVDV and the other half was administered a sham inoculation of sterile water 2 weeks before weaning. After weaning and arrival at the feedlot (day 0), all calves were commingled in a single pen with 4 calves PI with genotype 1b BVDV. Treatment groups were defined as follows: calves exposed to PI cattle before weaning and vaccinated against BVDV 2 weeks before weaning (group 2a; n = 37), calves exposed to PI cattle before weaning and not vaccinated against BVDV 2 weeks before weaning (group 2b; 26), calves not exposed to PI cattle before weaning and vaccinated against BVDV 2 weeks before weaning (group 2c; 37), and calves not exposed to PI cattle before weaning and not vaccinated against BVDV 2 weeks before weaning (group 2d; 38).

See Table 1 for remainder of key.

The mean (SD) weight and ADG for each treatment group throughout trial 2 were summarized (Table 5). Mean calf weight did not vary significantly among the treatment groups at any measurement during the 84-day feeding period. The ADG for steers was significantly (P < 0.001) greater than that for heifers. Calves exposed to PI cattle prior to weaning had a significantly (P = 0.043) greater ADG than did calves not exposed to PI cattle prior to weaning, regardless of whether they were vaccinated against BVDV 2 weeks before weaning. Calves vaccinated against BVDV 2 weeks before weaning had a significantly (P = 0.049) greater ADG than did calves not vaccinated against BVDV 2 weeks before weaning, regardless of exposure to PI cattle prior to weaning.

Table 5—

Mean (SD) weight and ADG for the calves of trial 2 on days 1 (processing), 28, 56, and 84 (just before transport for slaughter).

  Treatment group
VariableDay2a2b2c2d
Weight (kg)1230.53 (22.06)226.99 (18.72)228.06 (30.76)220.57 (16.74)
 28288.06 (31.51)277.41 (25.80)277.96 (38.55)267.49 (23.24)
 56324.45 (33.22312.13 (29.91)315.70 (42.35)304.55 (24.10)
 84356.88 (34.74)343.57 (29.42)348.99 (44.18)337.61 (26.57)
ADG (kg)282.06 (0.54)a1.80 (0.55)b1.78 (0.60)b1.71 (0.50)c
 561.68 (0.30)a1.52 (0.36)b1.57 (0.34)b1.52 (0.29)b
 841.50 (0.22)a1.39 (0.25)b1.44 (0.25)b1.41 (0.23)b

Within a variable and day, values with different superscript letters differ significantly (P < 0.05).

See Tables 2 and 4 for remainder of key.

Bovine viral diarrhea virus was isolated from all PI calves at all sample collections. At day 6, BVDV was isolated from nasal swab specimens of 3% (1/37), 0%, 3% (1/37), and 16% (6/38) of calves in treatment groups 2a, 2b, 2c, and 2d, respectively. At day 8, BVDV was isolated from nasal swab specimens of 3% (1/37), 0%, 3% (1/37), and 27% (10/38) of calves in treatment groups 2a, 2b, 2c, and 2d, respectively. At day 14, BVDV was isolated from 1 calf in groups 2a and 2c, and at day 28, BVDV was not isolated from any calf.

The geometric mean (SD) SNA titers against BVDV genotypes 1 and 2 on days −30 and 1 for each treatment group were summarized (Table 6). For the calves that were exposed to PI calves prior to weaning (groups 2a and 2b), the mean SNA titers against both genotype 1 and 2 BVDV were approximately 3 times as high, compared with those for the calves that were not exposed to PI calves prior to weaning (groups 2c and 2d).

Table 6—

Geometric mean (SD) SNA titers against BVDV genotypes 1 and 2 for the calves of trial 2 on days −30 and 1 (processing).

  Treatment group
GenotypeDay2a2b2c2d
1−306.9 (2.1)a7.5 (1.9)a2.3 (0.9)b2.2 (0.7)b
 18.3 (2.0)a*8.5 (2.1)a2.9 (1.6)b2.2 (0.7)b
2−305.8 (2.0)a6.1 (2.0)a2.0 (0.0)b2.0 (0.0)b
 17.1 (2.3)a*7.3 (2.5)a2.6 (1.6)b2.1 (0.5)b

Within a genotype and day, values with different superscript letters differ significantly (P < 0.05).

Within a genotype and treatment group, value differs significantly (P < 0.05) from that at day −30.

See Tables 3 and 4 for remainder of key.

Trial 3—During trial 3, 3 of 67 (4.5%) calves that were vaccinated against BVDV 3 weeks prior to weaning (group 3a) died because of BRD, whereas only 1 of 71 (1.4%) calves that were not vaccinated against BVDV 3 weeks prior to weaning (group 3b) died because of BRD. The morbidity, retreatment, and repull rates were summarized (Table 7). The morbidity, retreatment, and repull rates did not vary significantly between the treatment groups. However, morbidity rate was significantly (P = 0.001) associated with the farm from which the calves originated. Calves from farm 1 were 3.4 times (95% CI, 1.626 to 7.230) as likely to be treated as were calves from farm 2.

Table 7—

Morbidity, retreatment, and repull rates and risk ratios for 138 crossbred beef calves that were or were not vaccinated against BVDV 3 weeks prior to weaning and then commingled with PI cattle for a 168-day feeding period (trial 3).

OutcomeTreatment groupIncidence rate (%)Risk ratio (95% CI)P value
Morbidity3a32.83Referent
 3b42.251.50 (0.75–2.99)0.255
Retreatment3a27.27Referent
 3b23.330.812 (0.29–2.87)0.746
Repull3a9.10Referent
 3b23.333.04 (0.57–16.36)0.195

Calves in group 3a (n = 67) were vaccinated against BVDV 3 weeks before weaning, and calves in group 3b (71) were administered a sham inoculation of sterile water 3 weeks before weaning. After weaning and arrival at the feedlot (day 0), all calves were commingled in a single pen with 2 calves PI with genotype 2 BVDV.

See Table 1 for remainder of key.

The mean (SD) weight and ADG for each treatment group throughout trial 3 were summarized (Table 8). Mean weight on day 1 (during processing) did not differ significantly between calves in groups 3a and 3b. Similarly, the mean weight and ADG did not differ significantly between calves in groups 3a and 3b throughout the rest of the 168-day feeding period.

Table 8—

Mean (SD) weight and ADG for the calves of trial 3 on days 1 (processing), 28, 56, 84, 112, 140, and 168 (just before transport for slaughter).

  Treatment group
VariableDay3a3b
Weight (kg)1266.62 (36.55)256.88 (44.47)
 28292.16 (41.07)278.91 (50.24)
 56395.06 (49.50)377.73 (62.22)
 84444.30 (51.81)424.08 (65.95)
 112512.88 (50.38)490.64 (69.35)
 140567.72 (52.70)542.39 (70.73)
 168618.89 (55.94)595.65 (71.02)
ADG (kg)280.81 (0.42)0.68 (0.35)
 561.84 (0,27)1.76 (0.34)
 841.74 (0.32)1.66 (0.46)
 1122.46 (0.35)2.47 (0.39)
 1401.89 (0.33)1.78 (0.39)
 1681.60 (0.51)1.66 (0.44)

Within a variable and day, values did not differ significantly (P > 0.05).

See Tables 2 and 7 for remainder of key.

The geometric mean (SD) SNA titers against BVDV genotypes 1 and 2 on days −30 and 1 were summarized (Table 9). Following vaccination of the calves in group 3a, there was a significant increase in the SNA titers against both genotypes of BVDV. Following the sham inoculation of the calves in group 3b, the SNA titers against both genotypes of BVDV remained unchanged.

Table 9—

Geometric mean (SD) SNA titers against BVDV genotypes 1 and 2 for the calves of trial 3 on days −30 and 1 (processing).

  Treatment group
GenotypeDay3a3b
1−301.3 (1.5)1.4 (1.9)
 14.2 (1.0)a*1.4 (2.1)b
2−302.3 (2.0)1.6 (1.5)
 13.8 (0.4)a*1.6 (1.5)b

See Tables 6 and 7 for remainder of key.

Discussion

The 3 trials reported here replicated scenarios typical of the North American beef feedlot industry in that calves were weaned, commingled with calves from various locations, and transported to a feedlot where they were raised until they were marketed for slaughter. In this type of system, the risk of introducing a calf PI with BVDV to a group of potentially BVDV-naïve calves is high. Thus, it is important to elucidate the effect of exposure to PI cattle on the health and performance of non-PI cattle, and if this effect is detrimental, find ways to mitigate it.

Trial 1 was designed to reflect conditions under which beef calves are commonly managed in North America. Calves that had not been vaccinated for common BRD pathogens, including BVDV, and were at high risk of developing BRD because of stress associated with weaning, long-distance transport, handling and processing, and adjustment to a new housing and feeding environment were or were not vaccinated against BVDV at feedlot arrival and were or were not continuously commingled with PI calves. Results indicated that the morbidity rate for calves continuously exposed to PI cattle was approximately twice that of calves not exposed to PI cattle. This finding was not surprising because BVDV is an important pathogen associated with the BRD complex. Most of the calves that became ill during trial 1 were initially treated within 30 days after feedlot arrival and had clinical signs consistent with BRD. Bovine viral diarrhea virus causes substantial immunosuppression that facilitates the establishment of secondary respiratory tract pathogens.12 The increased morbidity rate for calves that were continuously exposed to PI cattle, compared with that for calves not exposed to PI cattle in this trial, was a finding consistent with the results of an epizootiological study5 of BVDV in feedlot cattle; however, results of another study13 suggest no association between morbidity rate and commingling with PI cattle. The conflicting findings are likely a result of differing calf management protocols among the studies.

In trial 1, calves exposed to PI cattle and administered a MLV BVDV vaccine at feedlot arrival had a lower morbidity rate than did calves exposed to PI cattle and not vaccinated against BVDV at feedlot arrival. Although administration of BRD vaccines to weaned calves prior to feedlot arrival (ie, preconditioning) is beneficial to the health of those calves during the feeding period,14 this type of preconditioning is not universally practiced. Investigators of another study15 reported that MLV BVDV vaccines can provide protection against BVDV infection within 7 days after administration. The results of trial 1 suggested that, although morbidity was not eliminated, it was substantially reduced by administration of an MLV BVDV vaccine to calves within 24 hours after feedlot arrival, even when those calves were continuously exposed to PI cattle. Moreover, prevention of exposure of feedlot cattle to PI cattle in conjunction with administration of an MLV BRD vaccine that included antigens for BVDV resulted in the lowest morbidity rate. Thus, identification and removal of PI cattle is an important management practice to help minimize the morbidity rate in feedlot cattle.

In trial 1, the ADG for calves continuously exposed to PI cattle was significantly lower than that for calves not exposed to PI cattle at 14 and 28 days after feedlot arrival, which coincided with the period during which most of the morbidity was observed. This finding was consistent with results of other studies,16–18 in which morbidity in general, and BRD in particular, had the greatest adverse effects on calf performance during the period immediately following feedlot arrival. A surprising finding in trial 1 was that ADG and final weight did not vary significantly among the treatment groups at the end of the feeding period. This suggested that the calves adjusted to the feedlot environment, developed immunity against circulating pathogens (including BVDV), and recovered from any illnesses during the feeding period, and the calves commingled with the PI cattle had compensatory weight gain that allowed them to match the weight gain of the calves not exposed to PI cattle.

Cross contamination between the treatment groups that were and were not exposed to PI cattle was of particular concern during trial 1. However, adequate biosecurity was maintained as evidenced by the failure to isolate BVDV from any of the calves not exposed to PI cattle (groups 1a and 1b) and the fact that none of the calves in group 1a (not exposed to PI cattle and not vaccinated against BVDV) developed substantial SNA titers against BVDV during the feeding period. Specific biosecurity measures that were instituted on the feedlot during trial 1 included prescribed traffic patterns, strategically located footbaths, and cleaning and disinfection of cattle-handling facilities between treatment groups.

Trial 2 was originally designed as a controlled trial in which BVDV-naïve calves would be systematically vaccinated against BVDV or administered a sham inoculation of sterile water 2 weeks before weaning, and at feedlot arrival, all calves would be commingled in a pen with 4 PI cattle for the duration of the feeding period. However, the initial PCR screening assay performed on pooled ear notch specimens failed to identify 4 PI calves in 2 of the 5 management groups of the herd of origin, and this failure was not detected until after the planned PI exposure trial had begun. Possible reasons for failure of the PCR assay performed on pooled ear notch specimens to identify PI cattle include laboratory error or levels of virus below the detectable limits in the skin specimens analyzed. We chose to continue the trial after the 4 PI calves from the herd of origin were identified; however, we adjusted the definitions for the treatment groups to control for exposure to PI cattle prior to weaning during data analysis.

Although morbidity rate and ADG did not differ significantly among the 4 treatment groups in trial 2, for the calves that were not exposed to PI cattle prior to weaning, those that were vaccinated against BVDV (group 2c) had a lower morbidity rate and higher ADG than did those that were not vaccinated against BVDV (group 2d), a finding that was consistent with results of other studies.19–21 Calves exposed to PI cattle prior to weaning had lower morbidity and mortality rates than did calves not exposed to PI cattle prior to weaning, regardless of vaccination status, a result that is consistent with findings of other studies22–24 and suggests that exposure of calves to BVDV before feedlot entry has a protective effect on health and performance during the feeding period. Additionally, the mean ADG for calves that were vaccinated against BVDV 2 weeks prior to weaning (groups 2a and 2c) was consistently higher than that for calves that were not vaccinated against BVDV 2 weeks prior to weaning (groups 2b and 2d) for each 28-day interval; thus, those calves weighed more at the end of the feeding period. Similarly, calves that were exposed to PI cattle before weaning (groups 2a and 2b) had a higher ADG than did calves that were not exposed to PI cattle before weaning (groups 2c and 2d). The lack of a significant interaction between exposure to PI cattle prior to weaning and administration of a BVDV vaccine 2 weeks before weaning suggested that the effect of PI exposure prior to weaning and preconditioning vaccine administration enhanced immunity against BVDV independently. This is biologically plausible because exposure of preweaned calves to various BVDV antigens should broaden their protection against the antigenically diverse strains of BVDV that they could be potentially exposed to in a commercial feedlot. In general, the results of trial 2 indicated that exposure of preweaned calves to BVDV either naturally via exposure to PI cattle or by vaccination had a protective effect on the health and performance of those calves when they were continuously commingled with PI cattle for the duration of the feeding period.

Other studies5,12,25–27 have yielded conflicting results regarding the effect of constant exposure to PI cattle on the health and performance of feedlot cattle. The results of trial 3 were similar to those of studies5,27,28 in which feedlot calves constantly exposed to PI cattle had increased morbidity rates and decreased weight gain, compared with those of feedlot calves not exposed to PI cattle. The magnitude of the effect of constant PI exposure on the health and performance of feedlot calves likely depends on multiple factors, including the virulence of the strain of BVDV to which the calves are exposed, the type and age of cattle, genetics, cattle management practices, and additional stressors such as duration of transport to the feedlot and the presence of other pathogens.3

Although the calves for trial 3 originated from 2 farms, preweaning management of those calves was similar because both farms were owned and operated by Michigan State University and the cattle health management was overseen by one of the investigators (DLG). All calves were the same sex and had a similar genetic background, age, and weight. The fact that all the calves in trial 3 originated from nearly identical management systems likely minimized the risk of disease transmission in the feedlot associated with commingling cattle from multiple sources.27 However, despite the similarities in preweaning management, calves that originated from farm 1 (the farm farthest from the research feedlot) were 3.4 times as likely to require treatment as were calves that originated from farm 2 (the farm closest to the research feedlot), regardless of vaccination status. Possible reasons why the morbidity rate differed between calves from farm 1 and farm 2 include differences in the nutrient availability and intake of dams and preweaned calves and the distance calves were transported (calves from farm 1 were transported 597 km [371 miles], whereas calves from farm 2 were only transported 224 km [139 miles]), factors that have been associated with BRD in feedlot cattle.14

Both cow-calf herds from which trial 3 calves originated were isolated from surrounding herds and had not had any significant infectious disease issues during the 10 years prior to initiation of the trial. Upon arrival at the research feedlot, the calves were isolated from other cattle at the feedlot; therefore, the risk of the trial calves being exposed to pathogens circulating among the other feedlot cattle that could have affected their health and performance should have been minimized. Generally, cattle infected with BVDV alone are subclinically affected or have few clinical signs29; however, cattle infected with BVDV and another secondary pathogen often develop severe clinical signs.30–32 It is likely that the absence of exposure of the trial calves to other pathogens contributed to the relatively low morbidity rates observed during trial 3.

Pathogenicity varies among BVDV strains.33–35 All PI cattle that were used in trial 3 were originally obtained from a feedlot and remained healthy throughout the trial, and information regarding the virulence of the BVDV strains that infected the PI cattle used as the source of virus exposure was unavailable.

All calves in trials 2 and 3 were administered an MLV vaccine that contained antigens for BVDV genotypes 1 and 2 within 24 hours after arrival at the feedlot. This is a common management practice on commercial feedlots regardless of whether calves have been vaccinated prior to feedlot arrival. Vaccination of the trial calves against BVDV soon after feedlot arrival likely mitigated the negative effects of constant exposure to PI cattle. Results of another study15 indicate that protection against BVDV challenge is induced within 72 hours after the administration of an MLV BVDV vaccine, and a similar outcome is observed for other BRD pathogens such as IBRV.36 Given that exposure to BVDV would not have been instantaneous or uniform among all the trial calves upon feedlot entry, it is possible that some of the calves that were not vaccinated before weaning had developed sufficient immunity from the MLV vaccine that was administered during processing to reduce the severity of disease when they became infected with BVDV.

Although significant differences in health and performance were not observed between the calves that were and were not vaccinated against BVDV 3 weeks before weaning in trial 3, those findings do not invalidate the findings of trials 1 and 2, which suggested that calves constantly exposed to PI cattle and not vaccinated against BVDV either at feedlot arrival or 2 weeks before weaning had increased morbidity rates and decreased performance, compared with those for calves that were vaccinated against BVDV. Moreover, even though the differences were not significant in trial 3, calves vaccinated against BVDV 3 weeks before weaning had a lower morbidity rate and higher ADG than did calves not vaccinated against BVDV 3 weeks before weaning, which suggested that vaccination of calves against BVDV before weaning is beneficial, especially when those calves are constantly exposed to PI cattle after entering the feedlot. Although vaccination of calves against BVDV before weaning or at feedlot arrival helped mitigate the risk of disease associated with commingling of those calves with PI cattle, it is likely that greater benefits would be realized from the identification and removal of PI cattle from the population.

Potential bias in the identification of sick cattle may have existed in all 3 trials. During all 3 trials, feedlot personnel were unaware of the vaccination status of individual calves; thus any bias would have been minimal. The potential for treatment bias was greater in trial 1, compared with that in trials 2 and 3, because the need to maintain biosecurity required that feedlot personnel were aware of which pen of trial calves contained the PI cattle. Thus, during trial 1, feedlot personnel might have inadvertently scrutinized the calves that were exposed to PI cattle to a greater extent than they did the calves not exposed to PI cattle, which might have resulted in the treatment of more calves that were exposed to PI cattle, compared with the number of calves treated that were not exposed to PI cattle. However, this bias would not have affected the observed difference between vaccinated and unvaccinated calves within each PI exposure group.

Results of the 3 trials reported here indicated that PI cattle adversely affect the health and performance of feedlot cattle. The magnitude of that adverse effect varied and was likely influenced by many factors such as the age, breed, nutritional status, and immune status of individual calves; environmental factors such as shipping, stocking density, and ventilation; and viral factors such as genotype and pathogenicity. The effect of exposure of feedlot calves to PI cattle was mitigated by exposure of those calves to BVDV before feedlot entry, either by natural exposure or vaccination. Although exposure of calves to BVDV prior to feedlot entry did not guarantee complete protection of those calves against BVDV infection or development of BRD, it did reduce the risk and severity of disease. These findings support the practice of vaccinating feedlot calves against BVDV as a method to mitigate the negative effects should those calves be exposed to PI cattle in the feedlot. Vaccination of feedlot calves against BVDV in combination with identification and removal of PI cattle from the population should minimize the effect of BVDV on the health and performance of feedlot cattle.

ABBREVIATIONS

ADG

Average daily gain

BRD

Bovine respiratory disease

BRSV

Bovine respiratory syncytial virus

BVDV

Bovine viral diarrhea virus

CI

Confidence interval

IBRV

Infectious bovine rhinotracheitis virus

MLV

Modified-live virus

PI

Persistently infected

PI3V

Parainfluenza type 3 virus

SNA

Serum neutralizing antibody

a.

Microsoft Excel 2003, Microsoft Corp, Redmond, Wash.

b.

Ultrabac 7/Somubac, Pfizer Animal Health, Madison, NJ.

c.

Cydectin Cattle Pour On, Pfizer Animal Health, Madison, NJ.

d.

Synovex-S, Pfizer Animal Health, Madison, NJ.

e.

Bovi-Shield IBR-PI3-BRSV, Pfizer Animal Health, Madison, NJ.

f.

Bovi-Shield 4, Pfizer Animal Health, Madison, NJ.

g.

Bovi-Shield GOLD FP 5, Pfizer Animal Health, Madison, NJ.

h.

One Shot, Pfizer Animal Health, Madison, NJ.

i.

Dectomax, Pfizer Animal Health, Madison, NJ.

j.

SAS, version 9.1, SAS Institute Inc, Cary, NC.

k.

STATA, version 10, Stata Corp, College Station, Tex.

References

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  • 2. Campbell JR. Effect of bovine viral diarrhea virus in the feedlot. Vet Clin North Am Food Anim Pract 2004; 20:3950.

  • 3. Grooms DL. Role of bovine viral diarrhea virus in the bovine respiratory disease complex. Bovine Pract 1998; 32(2):712.

  • 4. Baker JC. The clinical manifestations of bovine viral diarrhea infection. Vet Clin North Am Food Anim Pract 1995; 11:425445.

  • 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; 226:595601.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Taylor LF, Van Donkersgoed J, Dubovi EJ, et al. The prevalence of bovine viral diarrhea virus infection in a population of feedlot calves in western Canada. Can J Vet Res 1995; 59:8793.

    • Search Google Scholar
    • Export Citation
  • 7. Snedecor GW, Cocharan WG. The comparison of two samples. In: Statistical methods. 7th ed. Ames, Iowa: Iowa State Press, 1980;102105.

    • Search Google Scholar
    • Export Citation
  • 8. Crews D, Dikeman M, Dolezal H, et al. Animal evaluation. In: Hohenboken WD, ed. Guideline for uniform beef improvement programs. 8th ed. Athens, Ga: University of Georgia, 2002;1244.

    • Search Google Scholar
    • Export Citation
  • 9. Grooms DL, Brock KV, Ward LA. Detection of cytopathic bovine viral diarrheavirus in the ovaries of cattle following immunization with a modified live bovine viral diarrhea virus vaccine. J Vet Diagn Invest 1998; 10:130134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Corbett EM, Grooms DL, Bolin SR. Evaluation of skin samples for bovine viral diarrhea virus by use of reverse transcriptase polymerase chain reaction assay after vaccination of cattle with a modified-live bovine viral diarrhea virus vaccine. Am J Vet Res 2012; 73:319324.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Hardin JW, Hilbe JM. Generalized estimating equations. 2nd ed. Boca Raton, Fla: Chapman & Hall/CRC Press, 2012;1957.

  • 12. Ridpath J. The contribution of infections with bovine viral diarrhea viruses to bovine respiratory disease. Vet Clin North Am Food Anim Pract 2010; 26:335348.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. O'Connor AM, Sorden SD, Apley MD. Association between the existence of calves persistently infected with bovine viral diarrhea virus and commingling on pen morbidity in feedlot cattle. Am J Vet Res 2005; 66:21302134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Duff GC, Galyean ML. Board-invited review: recent advances in management of highly stressed, newly received feedlot cattle. J Anim Sci 2007; 85:823840.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Brock KV, Widel P, Walz P, et al. Onset of protection from experimental infection with type 2 bovine viral diarrhea virus following vaccination with a modified-live vaccine. Vet Ther 2007; 8:8896.

    • Search Google Scholar
    • Export Citation
  • 16. Smith RA. Impact of disease on feedlot performance: a review. J Anim Sci 1998; 76:272274.

  • 17. Wittum TE, Woollen NE, Perino LJ, et al. Relationships among treatment for respiratory tract disease, pulmonary lesions evident at slaughter, and rate of weight gain in feedlot cattle. J Am Vet Med Assoc 1996; 209:814818.

    • Search Google Scholar
    • Export Citation
  • 18. Gardner BA, Dolezal HG, Bryant LK, et al. Health of finishing steers: effects on performance, carcass traits, and meat tenderness. J Anim Sci 1999; 77:31683175.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Roeber DL, Speer NC, Gentry JG, et al. Feeder cattle health management: effects on morbidity rates, feedlot performance, carcass characteristics, and beef palatability. Prof Anim Sci 2001; 17:3944.

    • Search Google Scholar
    • Export Citation
  • 20. Kirkpatrick JG, Step DL, Payton ME, et al. Effect of age at the time of vaccination on antibody titers and feedlot performance in beef calves. J Am Vet Med Assoc 2008; 233:136142.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Fulton RW, Briggs RE, Ridpath JF, et al. Transmission of bovine viral diarrhea virus 1b to susceptible and vaccinated calves by exposure to persistently infected calves. Can J Vet Res 2005; 69:161169.

    • Search Google Scholar
    • Export Citation
  • 22. Martin SW, Bohac JG. The association between serological titers in infectious bovine rhinotracheitis virus, bovine viral diarrhea virus, parainfluenza-3 virus, respiratory syncytial virus and treatment for respiratory disease in Ontario feedlot calves. Can J Vet Res 1986; 50:351358.

    • Search Google Scholar
    • Export Citation
  • 23. Fulton RW, Cook BJ, Step DL, et al. Evaluation of health status of calves and the impact on feedlot performance: assessment of a retained ownership program for postweaning calves. Can J Vet Res 2002; 66:173180.

    • Search Google Scholar
    • Export Citation
  • 24. 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; 65:137142.

    • Search Google Scholar
    • Export Citation
  • 25. Burciaga-Robles LO, Krehbiel CR, Step DL, et al. Effects of exposure to calves persistently infected with bovine viral diarrhea virus type 1b and Mannheimia haemolytica challenge on animal performance, nitrogen balance, and visceral organ mass in beef steers. J Anim Sci 2010; 88:21792188.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Booker CW, Abutarbush SM, Morley PS, et al. The effect of bovine viral diarrhea virus infections on health and performance of feedlot cattle. Can Vet J 2008; 49:253260.

    • Search Google Scholar
    • Export Citation
  • 27. Hessman BE, Fulton RW, Sjeklocha DB, et al. Evaluation of the economic effects and the health and performance of the general cattle population after exposure to cattle persistently infected with bovine viral diarrhea virus in a starter feedlot. Am J Vet Res 2009; 70:7385.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Booker CW, Guichon PT, Jim GK, et al. Seroepidemiology of undifferentiated fever in feedlot calves in western Canada. Can Vet J 1999; 40:4048.

    • Search Google Scholar
    • Export Citation
  • 29. Baker JC. Bovine viral diarrhea virus. A review. J Am Vet Med Assoc 1987; 190:14491458.

  • 30. Wray C, Roeder PL. Effect of bovine virus diarrhoea-mucosal disease virus infection on Salmonella infection in calves. Res Vet Sci 1987; 42:213218.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Fulton RW, Step DL, Ridpath JF, et al. Response of calves persistently infected with noncytopathic bovine viral diarrhea virus (BVDV) subtype 1b after vaccination with heterologous BVDV strains in modified live virus vaccines and Mannheimia haemolytica bacterin-toxoid. Vaccine 2003; 21:29802985.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Potgieter LN, McCracken MD, Hopkins FM, et al. Experimental production of bovine respiratory tract disease with bovine viral diarrhea virus. Am J Vet Res 1984; 45:15821585.

    • Search Google Scholar
    • Export Citation
  • 33. Brodersen BW, Kelling CL. Effect of concurrent experimentally induced bovine respiratory syncytial virus and bovine viral diarrhea virus infection on respiratory tract and enteric diseases in calves. Am J Vet Res 1998; 59:14231430.

    • Search Google Scholar
    • Export Citation
  • 34. Potgieter LN, McCracken MD, Hopkins FM, et al. Comparison of the pneumopathogenicity of two strains of bovine viral diarrhea virus. Am J Vet Res 1985; 46:151153.

    • Search Google Scholar
    • Export Citation
  • 35. Walz PH, Bell TG, Grooms DL, et al. Platelet aggregation responses and virus isolation from platelets in calves experimentally infected with type I or type II bovine viral diarrhea virus. Can J Vet Res 2001; 65:241247.

    • Search Google Scholar
    • Export Citation
  • 36. Fairbanks KF, Campbell J, Chase CC. Rapid onset of protection against infectious bovine rhinotracheitis with a modified-live virus multivalent vaccine. Vet Ther 2004; 5:1725.

    • Search Google Scholar
    • Export Citation
  • 1. Lechtenberg KF, Smith RA, Stokka GL. Feedlot health and management. Vet Clin North Am Food Anim Pract 1998; 14:177197.

  • 2. Campbell JR. Effect of bovine viral diarrhea virus in the feedlot. Vet Clin North Am Food Anim Pract 2004; 20:3950.

  • 3. Grooms DL. Role of bovine viral diarrhea virus in the bovine respiratory disease complex. Bovine Pract 1998; 32(2):712.

  • 4. Baker JC. The clinical manifestations of bovine viral diarrhea infection. Vet Clin North Am Food Anim Pract 1995; 11:425445.

  • 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; 226:595601.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Taylor LF, Van Donkersgoed J, Dubovi EJ, et al. The prevalence of bovine viral diarrhea virus infection in a population of feedlot calves in western Canada. Can J Vet Res 1995; 59:8793.

    • Search Google Scholar
    • Export Citation
  • 7. Snedecor GW, Cocharan WG. The comparison of two samples. In: Statistical methods. 7th ed. Ames, Iowa: Iowa State Press, 1980;102105.

    • Search Google Scholar
    • Export Citation
  • 8. Crews D, Dikeman M, Dolezal H, et al. Animal evaluation. In: Hohenboken WD, ed. Guideline for uniform beef improvement programs. 8th ed. Athens, Ga: University of Georgia, 2002;1244.

    • Search Google Scholar
    • Export Citation
  • 9. Grooms DL, Brock KV, Ward LA. Detection of cytopathic bovine viral diarrheavirus in the ovaries of cattle following immunization with a modified live bovine viral diarrhea virus vaccine. J Vet Diagn Invest 1998; 10:130134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Corbett EM, Grooms DL, Bolin SR. Evaluation of skin samples for bovine viral diarrhea virus by use of reverse transcriptase polymerase chain reaction assay after vaccination of cattle with a modified-live bovine viral diarrhea virus vaccine. Am J Vet Res 2012; 73:319324.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Hardin JW, Hilbe JM. Generalized estimating equations. 2nd ed. Boca Raton, Fla: Chapman & Hall/CRC Press, 2012;1957.

  • 12. Ridpath J. The contribution of infections with bovine viral diarrhea viruses to bovine respiratory disease. Vet Clin North Am Food Anim Pract 2010; 26:335348.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. O'Connor AM, Sorden SD, Apley MD. Association between the existence of calves persistently infected with bovine viral diarrhea virus and commingling on pen morbidity in feedlot cattle. Am J Vet Res 2005; 66:21302134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Duff GC, Galyean ML. Board-invited review: recent advances in management of highly stressed, newly received feedlot cattle. J Anim Sci 2007; 85:823840.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Brock KV, Widel P, Walz P, et al. Onset of protection from experimental infection with type 2 bovine viral diarrhea virus following vaccination with a modified-live vaccine. Vet Ther 2007; 8:8896.

    • Search Google Scholar
    • Export Citation
  • 16. Smith RA. Impact of disease on feedlot performance: a review. J Anim Sci 1998; 76:272274.

  • 17. Wittum TE, Woollen NE, Perino LJ, et al. Relationships among treatment for respiratory tract disease, pulmonary lesions evident at slaughter, and rate of weight gain in feedlot cattle. J Am Vet Med Assoc 1996; 209:814818.

    • Search Google Scholar
    • Export Citation
  • 18. Gardner BA, Dolezal HG, Bryant LK, et al. Health of finishing steers: effects on performance, carcass traits, and meat tenderness. J Anim Sci 1999; 77:31683175.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Roeber DL, Speer NC, Gentry JG, et al. Feeder cattle health management: effects on morbidity rates, feedlot performance, carcass characteristics, and beef palatability. Prof Anim Sci 2001; 17:3944.

    • Search Google Scholar
    • Export Citation
  • 20. Kirkpatrick JG, Step DL, Payton ME, et al. Effect of age at the time of vaccination on antibody titers and feedlot performance in beef calves. J Am Vet Med Assoc 2008; 233:136142.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Fulton RW, Briggs RE, Ridpath JF, et al. Transmission of bovine viral diarrhea virus 1b to susceptible and vaccinated calves by exposure to persistently infected calves. Can J Vet Res 2005; 69:161169.

    • Search Google Scholar
    • Export Citation
  • 22. Martin SW, Bohac JG. The association between serological titers in infectious bovine rhinotracheitis virus, bovine viral diarrhea virus, parainfluenza-3 virus, respiratory syncytial virus and treatment for respiratory disease in Ontario feedlot calves. Can J Vet Res 1986; 50:351358.

    • Search Google Scholar
    • Export Citation
  • 23. Fulton RW, Cook BJ, Step DL, et al. Evaluation of health status of calves and the impact on feedlot performance: assessment of a retained ownership program for postweaning calves. Can J Vet Res 2002; 66:173180.

    • Search Google Scholar
    • Export Citation
  • 24. 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; 65:137142.

    • Search Google Scholar
    • Export Citation
  • 25. Burciaga-Robles LO, Krehbiel CR, Step DL, et al. Effects of exposure to calves persistently infected with bovine viral diarrhea virus type 1b and Mannheimia haemolytica challenge on animal performance, nitrogen balance, and visceral organ mass in beef steers. J Anim Sci 2010; 88:21792188.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Booker CW, Abutarbush SM, Morley PS, et al. The effect of bovine viral diarrhea virus infections on health and performance of feedlot cattle. Can Vet J 2008; 49:253260.

    • Search Google Scholar
    • Export Citation
  • 27. Hessman BE, Fulton RW, Sjeklocha DB, et al. Evaluation of the economic effects and the health and performance of the general cattle population after exposure to cattle persistently infected with bovine viral diarrhea virus in a starter feedlot. Am J Vet Res 2009; 70:7385.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Booker CW, Guichon PT, Jim GK, et al. Seroepidemiology of undifferentiated fever in feedlot calves in western Canada. Can Vet J 1999; 40:4048.

    • Search Google Scholar
    • Export Citation
  • 29. Baker JC. Bovine viral diarrhea virus. A review. J Am Vet Med Assoc 1987; 190:14491458.

  • 30. Wray C, Roeder PL. Effect of bovine virus diarrhoea-mucosal disease virus infection on Salmonella infection in calves. Res Vet Sci 1987; 42:213218.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Fulton RW, Step DL, Ridpath JF, et al. Response of calves persistently infected with noncytopathic bovine viral diarrhea virus (BVDV) subtype 1b after vaccination with heterologous BVDV strains in modified live virus vaccines and Mannheimia haemolytica bacterin-toxoid. Vaccine 2003; 21:29802985.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Potgieter LN, McCracken MD, Hopkins FM, et al. Experimental production of bovine respiratory tract disease with bovine viral diarrhea virus. Am J Vet Res 1984; 45:15821585.

    • Search Google Scholar
    • Export Citation
  • 33. Brodersen BW, Kelling CL. Effect of concurrent experimentally induced bovine respiratory syncytial virus and bovine viral diarrhea virus infection on respiratory tract and enteric diseases in calves. Am J Vet Res 1998; 59:14231430.

    • Search Google Scholar
    • Export Citation
  • 34. Potgieter LN, McCracken MD, Hopkins FM, et al. Comparison of the pneumopathogenicity of two strains of bovine viral diarrhea virus. Am J Vet Res 1985; 46:151153.

    • Search Google Scholar
    • Export Citation
  • 35. Walz PH, Bell TG, Grooms DL, et al. Platelet aggregation responses and virus isolation from platelets in calves experimentally infected with type I or type II bovine viral diarrhea virus. Can J Vet Res 2001; 65:241247.

    • Search Google Scholar
    • Export Citation
  • 36. Fairbanks KF, Campbell J, Chase CC. Rapid onset of protection against infectious bovine rhinotracheitis with a modified-live virus multivalent vaccine. Vet Ther 2004; 5:1725.

    • Search Google Scholar
    • Export Citation

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