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  • 24. Burton JL, Burnside EB, Kennedy BW, et al. Antibody responses to human erythrocytes and ovalbumin as marker traits of disease resistance in dairy calves. J Dairy Sci 1989; 72: 12521265.

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  • 25. Ellsworth MA, Brown MJ, Fergen BJ, et al. Safety of modified-live combination vaccine against respiratory and reproductive diseases in pregnant cows. Vet Ther 2003; 4: 120127.

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  • 26. Kendrick JW, Franti CE. Bovine viral diarrhea: decay of colostrum-confirmed antibody in the calf. Am J Vet Res 1974; 35: 589591.

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  • 28. Schefers J, Munoz-Zanzi C, Collins JE, et al. Serological evaluation of precolostral serum samples to detect bovine viral diarrhea virus infections in large commercial dairy herds. J Vet Diagn Invest 2008; 20: 625628.

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  • 29. Kleiboeker SB, Lee SM, Jones CA, et al. Evaluation of shedding of bovine herpesvirus 1, bovine viral diarrhea virus 1, and bovine viral diarrhea virus 2 after vaccination of calves with a multivalent modified-live virus vaccine. J Am Vet Med Assoc 2003; 222: 13991403.

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  • 30. USDA APHIS Veterinary Services. Exemption from label warning concerning the use of bovine rhinotracheitis vaccine, modified live virus in pregnant cows or in calves nursing pregnant cows under 9 code of federal regulations 122.7(e). Veterinary Services memorandum No. 800.110. 2004.

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  • 31. Chase CCL, Chase SK, Fawcett L. Trends in the BVDV serological response in the upper Midwest. Biologicals 2003; 31: 145151.

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  • 33. 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. J Am Vet Med Assoc 2002; 221: 678685.

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  • 34. 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: 643649.

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  • 35. Ridpath JE, Neill JD, Endsley J, et al. Effect of passive immunity on the development of a protective immune response against bovine viral diarrhea virus in calves. Am J Vet Res 2003; 64: 6569.

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Anti-bovine herpesvirus and anti-bovine viral diarrhea virus antibody responses in pregnant Holstein dairy cattle following administration of a multivalent killed virus vaccine

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  • 1 Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA 19348.
  • | 2 Department of Mathematics, College of Arts and Sciences, West Chester University, West Chester, PA 19383.
  • | 3 Walmoore Dairy Inc, PO Box 158, Chatham, PA 19318.
  • | 4 Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.
  • | 5 Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA 19348.

Abstract

OBJECTIVE To determine the effect of a commercially available multivalent killed virus vaccine on serum neutralizing (SN) and colostrum neutralizing (CN) antibodies against bovine herpesvirus (BHV) type 1 and bovine viral diarrhea virus (BVDV) types 1 and 2 in pregnant dairy cattle.

ANIMALS 49 Holstein dairy cattle.

PROCEDURES 25 cattle were vaccinated (IM injection) at least 60 days prior to calving (ie, at the end of the lactation period or according to the expected calving date for heifers) and again 5 weeks later. The remaining 24 cattle were not vaccinated (control group). Titers of SN antibodies were measured at the 5-week time point. Titers of SN and CN antibodies were measured at parturition.

RESULTS 5 weeks after initial vaccination, titers of SN antibodies against BHV-1 and BVDV types 1 and 2 were 1:512, 1:128, and 1:2,048, respectively, in vaccinates and 1:64, 1:128, and 1:64, respectively, in unvaccinated controls. Equivalent SN antibody titers at parturition were 1:256, 1:64, and 1:512, respectively, in vaccinates and 1:128, 1:128, and 1:64, respectively, in controls. Median titers of CN antibodies against BHV-1 and BVDV types 1 and 2 were 1:1,280, 1:10,240, and 1:20,480, respectively, in vaccinates and 1:80, 1:1,280, and 1:2,560, respectively, in controls.

CONCLUSIONS AND CLINICAL RELEVANCE Titers of antibodies against viral respiratory pathogens were significantly enhanced in both serum (BHV-1 and BVDV type 2) and colostrum (BHV-1 and BVDV types 1 and 2) in cattle receiving a killed virus vaccine (with no adverse reactions) before parturition. To maximize protection of bovine neonates, this method of vaccination should be considered.

Abstract

OBJECTIVE To determine the effect of a commercially available multivalent killed virus vaccine on serum neutralizing (SN) and colostrum neutralizing (CN) antibodies against bovine herpesvirus (BHV) type 1 and bovine viral diarrhea virus (BVDV) types 1 and 2 in pregnant dairy cattle.

ANIMALS 49 Holstein dairy cattle.

PROCEDURES 25 cattle were vaccinated (IM injection) at least 60 days prior to calving (ie, at the end of the lactation period or according to the expected calving date for heifers) and again 5 weeks later. The remaining 24 cattle were not vaccinated (control group). Titers of SN antibodies were measured at the 5-week time point. Titers of SN and CN antibodies were measured at parturition.

RESULTS 5 weeks after initial vaccination, titers of SN antibodies against BHV-1 and BVDV types 1 and 2 were 1:512, 1:128, and 1:2,048, respectively, in vaccinates and 1:64, 1:128, and 1:64, respectively, in unvaccinated controls. Equivalent SN antibody titers at parturition were 1:256, 1:64, and 1:512, respectively, in vaccinates and 1:128, 1:128, and 1:64, respectively, in controls. Median titers of CN antibodies against BHV-1 and BVDV types 1 and 2 were 1:1,280, 1:10,240, and 1:20,480, respectively, in vaccinates and 1:80, 1:1,280, and 1:2,560, respectively, in controls.

CONCLUSIONS AND CLINICAL RELEVANCE Titers of antibodies against viral respiratory pathogens were significantly enhanced in both serum (BHV-1 and BVDV type 2) and colostrum (BHV-1 and BVDV types 1 and 2) in cattle receiving a killed virus vaccine (with no adverse reactions) before parturition. To maximize protection of bovine neonates, this method of vaccination should be considered.

Respiratory tract disease remains a major problem in the dairy industry. It continues to cause morbidity, death, and economic loss due to pneumonia. According to the USDA National Animal Health Monitoring System, the mortality rate (21% to 24%) associated with preweaned calf pneumonia has been, for the most part, unchanged since the early 1990s.1 However, during the same period, the mortality rate associated with weaned calf pneumonia increased substantially from 35% to 47%.1

The economic cost of dairy calf pneumonia includes expenses associated with measures of prevention and treatment as well as losses associated with lower productivity. The National Animal Health Monitoring System estimates the cost of respiratory tract disease to be as high as $16/unweaned calf1 and $2/weaned calf.2,3 More importantly, perhaps, are the significant negative effects on future productivity of dairy animals. It has been reported that a single episode of pneumonia during the first 6 months after birth results in slower growth rate4 and decreased productivitya as an adult bovid.

Commercial vaccines against bovine respiratory tract diseases are commonly administered to cattle with the intention of inducing immediate antibody protection. The most commonly used vaccines are multivalent and contain several viral antigens or bacterins that supply bacterial antigens. Another important role of vaccines is to supply antibody protection in colostrum to the offspring. Colostrum quality is dependent on the abundance of antibodies passed from the cow's blood into the mammary glands near the time of parturition.5–7 In cattle, the partitioning of antibodies to colostrum begins 2 to 3 weeks prior to parturition, and the amount and specificity of the antibodies transferred are dependent on the exposure of the dam to pathogenic agents.8–11 Although it is assumed that the dam can also produce adequate colostral antibodies after natural exposure, vaccinating dairy cattle prior to parturition should promote the production of higher quality colostrum.

One major problem with vaccination of pregnant cows is abortion.12 Vaccine manufacturers are required to state on labels the potential risks related to fetal loss when vaccines are used in pregnant immune-naïve cows. Fetal loss occurs more often after administration of a modified-live virus vaccine rather than a vaccine product containing killed viral antigens.12 Because of the potential for fetal loss, many veterinarians have advised producers to cease vaccinating pregnant cows prior to calving and vaccinate instead in the immediate postpartum period. In the United States, it is now standard protocol to vaccinate dairy cows against bovine respiratory disease starting at least 3 weeks after parturition. It is possible that the desire to protect unborn calves by not vaccinating cows just prior to parturition has resulted in lower quality colostrum in terms of both quantity and antigen specificity of colostral antibodies. Additionally, in herds without a current vaccination program, it could be detrimental to fetal survival if a program is first initiated with use of modified-live virus vaccines. Killed virus vaccines provide a safer option in pregnant cattle while also improving colostrum quality; a killed virus vaccination protocol could be initiated in unvaccinated herds with little concern regarding fetal loss.

The aim of the study reported here was to evaluate the antibody response in serum and colostrum of pregnant cattle on a commercial dairy farm following administration of a multivalent killed virus vaccine containing the viral antigens BHV-1, BVDV types 1 and 2, parainfluenza type 3, and BRSV plus bacterins for Leptospira serovars Canicola, Grippotyphosa, Hardjo, Icterohemorrhagiae, and Pomona. The focus was respiratory tract disease, and serologic responses to leptospiral bacterins were not evaluated. Parainfluenza type 3 is generally regarded as being of low pathogenicity; therefore, serologic evaluation was not pursued. In the case of BRSV, a study13 has revealed how difficult it is to interpret antibody titers following vaccination and what constitutes a protective titer is uncertain. Therefore, measurements were restricted to vaccine-associated antigens for those principal major pathogens that lead to fairly predictable antibody responses (ie, BHV-1, BVDV type 1, and BVDV type 2). Our hypothesis was that vaccination of dairy cattle after cessation of lactation and just prior to parturition would increase titers of serum antibodies against specific antigens, which would in turn translate into increases in titers of the same antibodies in the colostrum at parturition. Considering that all vaccinated animals received a vaccine they had never been previously administered, a secondary aim was to monitor the effect of vaccination on fetal loss.

Materials and Methods

Farm and management

This study was performed at a 600-cow dairy farm in southeast Pennsylvania. Owner consent was obtained, and the study was approved by the Veterinary School's Privately Owned Animal Protocol procedure. The test herd was enrolled in a yearly program to receive modified-live virus vaccines. On the farm, the standard protocol included vaccination of dairy cows against respiratory tract disease starting at least 3 weeks after parturition. Cattle were housed in a 6-row, open ridge, free-stall barn with curtain sidings, canvas mattresses, rubber flooring in the alleys, automatic alley scrapers, and open-rail feed bunks. For management purposes, this dairy herd was kept in 5 groups according to age, parturition status, or milk production (ie, cows of any parity that had recently given birth, and cows with low, medium, or high milk production). Cows in lactation were milked twice a day; all cattle were fed a total mixed ration and had ad libitum access to water. In addition, nonlactating cows had access to hay.

Once weekly, pregnant cattle that were at least 60 days from calving were identified. For cattle other than pregnant heifers, milking was abruptly stopped at that time. Those cows were administered an intramammary antimicrobial treatment into all lactating mammary glands, after which each teat was dipped with a topical teat sealant (ie, dry cow treatment). Standard protocol required that all cows receive 2 vaccines at this time: one contained a gram-negative core antigen and the other was a multivalent bacterial toxoid.

Animals

To conduct the study within the allowed budget and in a reasonable time frame, 49 Holstein cattle were identified as study participants. These animals had previously undergone the dairy herd's routine vaccination protocol for the viruses of interest and had received their first modified-live virus vaccination at 4 months of age, followed by a booster at 5 months, a second booster at the time of breeding (12 to 15 months), and annually thereafter 3 weeks after parturition. On the day of each week that dry cow treatment was undertaken, the cows and pregnant heifers that were at least 60 days from the expected calving date were alternately assigned to receive vaccination with the study vaccine or remain unvaccinated (no sham vaccine was used). Over a period of 16 weeks, 25 cattle were assigned to the vaccinated group and 24 cattle were assigned to the control group. The dairy herd's standard vaccine protocol was changed so that vaccinates received a multivalent killed virus vaccineb at this time (approx 8 weeks prior to calving). Cattle in the vaccinated group received a booster vaccination 5 weeks after the first vaccine administration (approx 3 weeks prior to calving). The vaccine was administered into the cervical musculature at a clean, dry location. Animals were monitored daily, and any adverse reactions were noted.

Analysis of serum antibody titers

Blood samples (10 mL each) were collected by coccygeal venipuncture from all 49 animals; each sample was collected into a plain evacuated tube.c A blood sample was obtained from vaccinated cattle immediately before the second vaccination (booster dose administered 5 weeks after initial vaccination) and again on the day of parturition (within 12 hours after calving). A blood sample was obtained from control cattle in a similar manner (ie, 5 weeks after initial enrollment in the study and again within 12 hours after calving on the day of parturition). Blood samples were allowed to coagulate, then refrigerated at 4.4°C; clots were removed within 24 hours after collection. Serum was recovered by centrifugation at 4,500 × g and stored frozen at −20°C. Titers of SN antibodies against BHV-1 and BVDV types 1 and 2 were measured by use of a varying serum-constant virus dilution method.14,15 Briefly, serial 2-fold dilutions of each serum sample were combined with equal volumes of standardized reference strains of BHV-1, BVDV type 1, or BVDV type 2. After being incubated for 1 hour at 35° to 37°C, 0.2 mL of the virus-serum mixture, containing 50× to 250× the reference virus TCID50, was incubated on a bovine turbinate cell lined for a minimum of 5 days at 35° to 37°C. The SN antibody titer was calculated as the reciprocal of the highest dilution that resulted in 50% inhibition of the cytopathic effect.

Analysis of colostral antibody titers

A colostrum sample (10 mL) was collected separately from each of the 49 animals at the first postcalving milking (ie, within 12 hours after calving). Colostrum samples were initially refrigerated at 4.4°C for 2 to 3 hours, and then stored frozen at −20°C until analysis. Colostrum neutralizing antibody titers were measured by a method analogous to that described for SN antibody titer measurement.

Statistical analysis

Statistical analyses were performed with the aid of commercially available software.e,f Group characteristics (age and parity at the start of the study, and milk production as 305-day mature equivalent from the previous lactation) were tested for normality by means of a Shapiro-Wilk test. Normally distributed data were compared by means of a 2-sample t test, and data that were not normally distributed were compared by means of the nonparametric Wilcoxon rank sum test.f Differences between vaccinated and unvaccinated cattle with regard to SN antibody titers at the time of booster vaccination and on the day of parturition and CN antibody titers (in colostrum obtained from the first postcalving milking) were assessed. The outcomes of interest were titers of SN and CN antibodies against BHV-1, BVDV type 1, and BVDV type 2. Because the primary questions of interest required comparison of specific titers in serum and colostrum at the 3 time points, individual tests between groups were performed at each time point.

The individual titers measured at each time point were normalized through a binary logarithmic transformation. In some instances, even after transformation, the normality of titer distributions within groups was questionable. Therefore, for each comparison, both the parametric Student t test and the nonparametric Wilcoxon rank sum (Mann-Whitney U) test were performed.e Results obtained with transformed data and a parametric analysis were similar to those derived from the nonparametric method; even though the Wilcoxon rank sum test has less power, it does not require distributional assumptions, and so the results of the nonparametric test on untransformed data are reported here. In addition to between-group comparisons of antibody titers, any within-group comparisons were made via the same statistical approach. Values of P ≤ 0.05 were considered significant. No fetal loss occurred in either group, so no comparisons were required.

Results

Study animals were monitored daily, and any adverse events were noted on individual cow cards in the herd's computerized record system.g Each cow card was examined and relevant data collected at the end of the study. Samples of blood and colostrum were obtained from all 49 cattle at each of the 3 time points. Data regarding age and parity were known for all cattle; however, because heifers were included in the study groups, milk production data were not available for each animal.

Group characteristics

Even though all cattle were enrolled into the study when they were at least 60 days from their expected calving date and were randomly assigned to the control or vaccinated group, more heifers were allocated to the control group (n = 12) than the vaccinated group (0). As a result, age (control group mean age, 33 months [median age, 27 months; IQR, 22 to 45 months; range, 20 to 63 months); vaccinated group mean age, 42 months [median age, 35 months; IQR, 32 to 46 months; range, 29 to 92 months]) and parity (control group mean parity, 1 [median, 0.5; IQR, 0 to 2; range, 0 to 3]; vaccinated group mean parity, 2 [median, 1; IQR, 1 to 2; range, 1 to 4]) distributions of the 2 groups were significantly (P = 0.02 and P = 0.01, respectively) different. With regard to cows with parity ≤ 1 for which milk production data (305-day mature equivalent) were available, there was no significant (P = 0.46) difference between the control (10,795 ± 1,739 kg [n = 12]) and vaccinated (11,281 ± 1,914 kg [25]) groups.

Titers of SN antibodies at time of booster vaccination

At 5 weeks after the initial vaccination or enrollment into the study (in the case of controls), median titers of SN antibodies against BHV-1, BVDV type 1, and BVDV type 2 were 1:64, 1:128, and 1:64, respectively, for the control group and in comparison, 1:512 (P < 0.001), 1:128 (P = 0.603), and 1:2,048 (P = 0.001), respectively, for the vaccinated group. The vaccinated group had significantly higher SN anti–BHV-1 and anti–BVDV type 2 antibody titers at this time point, compared with findings for the control group. However, SN anti–BVDV type 1 antibody titers were not significantly different between the vaccinated and control group (Table 1).

Table 1—

Titers of SN and CN antibodies against BHV-1, BVDV type 1, and BVDV type 2 in 49 dairy cattle that were or were not vaccinated with a multivalent killed virus vaccine first at 8 weeks and again at 3 weeks prior to calving (booster vaccination).

 SN antibody titer   
 3 weeks prior to parturitionDay of parturitionCN antibody titer
VirusControl (n = 24)Vaccinated (n = 25)P value*Control (n = 24)Vaccinated (n = 25)P value*Control (n = 24)Vaccinated (n = 25)P value*
BHV-11:64 (1:8–1:1,024)1:512 (1:32–1:4,096)< 0.0011:128 (1:16–1:1,024)1:256 (1:64–1:2,048)< 0.0011:80 (1:10–1:5,120)1:1,280 (1:40–1:2,560)< 0.001
BVDV type 11:128 (1:2–1:4,096)1:128 (1:16–1:4,096)0.6031:128 (1:8–1:2,048)1:64 (1:16–1:2,048)0.7081:1,280 (1:160–1:20,480)1:10,240 (1:1,280–1:20,480)< 0.001
BVDV type 21:64 (1:2–1:4,096)1:2,048 (1:4–1:4,096)0.0011:64 (1:2–1:4,096)1:512 (1:16–1:4,096)0.0021:2,560 (1:160–1:20,480)1:20,480 (1:1,280–1:20,480)0.001

Values are median (range).

Titers for antibodies against a given virus at a given time point were compared; a value of P < 0.05 was considered significant (nonparametric Mann-Whitney U test).

Cattle were assigned to either the vaccinated group or control group when they were at least 60 days from their expected calving date. Cattle in the vaccinated group received a dose of the vaccine IM at this time point and a booster vaccination 5 weeks later (approx 3 weeks prior to calving); cattle in the control group remained untreated (no sham vaccine administered). A blood sample was collected from each animal at 3 weeks prior to (before administration of the booster vaccine in vaccinates) and within 12 hours after parturition. A sample of colostrum was obtained during the first postcalving milking (within 12 hours after calving).

Titers of SN antibodies on day of parturition

On the day of parturition (within 12 hours after calving), median titers of SN antibodies against BHV-1, BVDV type 1, and BVDV type 2 were 1:128, 1:128, and 1:64, respectively, for the control group and in comparison, 1:256 (P < 0.001), 1:64 (P = 0.708), and 1:512 (P = 0.002), respectively, for the vaccinated group. Analogous to findings at the time immediately before the booster vaccination or 5 weeks after enrollment in the study (ie, 3 weeks prior to calving), the vaccinated group had significantly higher SN anti–BHV-1 and anti–BVDV type 2 antibody titers at parturition, compared with findings for the control group. However, SN anti–BVDV type 1 antibody titers were not significantly different between the vaccinated and control group (Table 1).

Titers of CN antibodies in samples from the first postcalving milking

Median titers of CN antibodies against BHV-1, BVDV type 1, and BVDV type 2 were 1:80, 1:1,280, and 1:2,560, respectively, for the control group and in comparison, 1:1,280 (P < 0.001), 1:10,240 (P < 0.001), and 1:20,480 (P = 0.001), respectively, for the vaccinated group. In contrast to SN antibody titers at parturition, the vaccinated group had significantly higher titers of CN antibodies against all 3 viruses, compared with findings for the control group (Table 1).

Within-group comparisons

Descriptive statistics indicated that the group compositions were different in terms of age and parity, with more heifers in the control group. Therefore, to assess whether this significantly affected interpretation of the study data, within-group comparisons of SN and CN antibody titers were made by comparing results for young (parity 0 or 1) and older (parity > 1) animals. In the vaccinated group, there were 15 young cattle and 10 older cattle; in the control group, there were 12 young cattle and 12 older cattle. With 1 exception, the pattern of differences observed between the young and older cattle in both the control group and vaccinated group were the same (Table 2). With regard to any of the titers of SN or CN antibodies against BVDV types 1 or 2, there were no significant within-group differences. For young animals, (parity 0 or 1) BVDV type 2 but not BVDV type 1, SN antibody titers in vaccinated cattle were significantly higher than those in the young control animals. In older cows (parity > 1), SN BVDV type 2 titers at calving were significantly higher in the vaccinated group than in older control cows. Median SN BVDV type 2 titers were also higher in older vaccinated cows at the time of booster vaccination, but this effect was not significant. Within-group and between group SN titer patterns similar to that for BVDV type 2 were found for titers of SN anti–BHV-1 antibodies at 5 weeks after the initial vaccination or enrollment into the study and on the day of parturition (within 12 hours after calving), but at each time point titers for both young and older vaccinated cows were significantly higher than their control counterparts. Titers of CN antibodies against BHV-1 in young vaccinates were the same as those of the older vaccinates; however, young animals in the control group had titers of CN antibodies against BHV-1 that were significantly (P = 0.004) lower than those of their older counterparts. Colostrum neutralizing antibody titers in both young (P < 0.001) and older (P = 0.011) control animals were significantly lower than those observed in the young and older vaccinated animals. Colostrum neutralizing antibody titers against both BVDV types 1 and 2 were significantly higher in young vaccinates, compared with young controls. Although median titers of CN antibodies against BVDV types 1 and 2 were also higher in older vaccinated cows than in older control cows, the differences were not significant.

Table 2—

Effect of parity (0 or 1 [n = 12 for the control group and 15 for the vaccinated group] or > 1 [12 for the control group and 10 for the vaccinated group]) on titers of SN and CN antibodies against BHV-1, BVDV type 1, and BVDV type 2 in the 49 dairy cattle in Table 1 that were or were not vaccinated with a multivalent killed virus vaccine first at 8 weeks and again at 3 weeks prior to calving (booster vaccination).

  SN antibody titer   
  3 weeks prior to parturitionDay of parturitionCN antibody titer
VirusParityControlVaccinatedP value*ControlVaccinatedP value*ControlVaccinatedP value*
BHV-10 or 11:64 (1:8–1:256)1:1,280 (1:40–1:2,560)< 0.0011:64 (1:16–1:128)1:256 (1:64–1:2,048)< 0.0011:40 (1:10–1:320)1:1,280 (1:40–1:2,560)< 0.001
 > 11:192 (1:64–1:1,024)1:1,280 (1:640–1:2,560)0.0051:128 (1:32–1:1,024)1:512 (1:128–1:2,048)0.0081:240 (1:40–1:5,120)1:1,280 (1:640–1:2,560)0.011
BVDV type 10 or 11:256 (1:2–1:1,024)1:64 (1:16–1:4,096)0.5821:128 (1:64–1:2,048)1:64 (1:16–1:2,048)0.1651:640 (1:160–1:2,560)1:10,240 (1:1,280–1:20,480)< 0.001
 > 11:128 (1:4–1:4,096)1:576 (1:12–1:2,048)0.2721:96 (1:8–1:512)1:128 (1:16–1:2,048)0.4411:3,840 (1:320–1:20,480)1:10,240 (1:1,280–1:20,480)0.300
BVDV type 20 or 11:128 (1:4–1:256)1:2,048 (1:8–1:4,096)0.0021:64 (1:2–1:512)1:384 (1:16–1:4,096)0.0331:2,560 (1:160–1:20,480)1:20,480 (1:2,560–1:20,480)0.022
 > 11:48 (1:2–1:4,096)1:2,048 (1:4–1:4,096)0.1071:192 (1:92–1:4,096)1:2,560 (1:32–1:4,096)0.0181:12,800 (1:160–1:20,480)1:20,480 (1:1,280–1:20,4800.143

Values are median (range).

Titers for antibodies against a given virus at a given time point were compared in vaccinated and control cattle by parity 0 or 1 (younger) or > 1 (older); a value of P < 0.05 was considered significant (nonparametric Mann-Whitney U test).

See Table 1 for key.

Fetal loss and adverse reactions

No adverse reactions of any kind were reported for any animal in either group. All cattle calved uneventfully.

Discussion

In the dairy industry, many strategies are used to control calfhood respiratory tract disease, the most important of which is prevention. It is common practice to use biologics to vaccinate against the pathogens commonly believed to cause respiratory tract disease. However, what is not clear is which group of animals should be targeted for preventive vaccination to be most effective. Generally, dairy calves are vaccinated at birth and frequently thereafter until adulthood. Depending on the age at first vaccination, method of vaccination, and biologics used, studies have variously shown vaccination, even in the presence of maternal antibodies, to be beneficial,11,16–19 noneffective,20–22 or even detrimental.23 An alternative strategy is to vaccinate late-term pregnant cows during the prepartum period with the aim of increasing concentrations of maternal antibodies in colostrum. The disadvantage of this approach is that use of biologics in the prepartum period may cause harm to the dam or offspring.12

Little research has been performed to determine the impact of prepartum vaccination of dairy cattle on the production of specific colostral antibodies. Previous reports5,9 have suggested that cattle with higher serum antibody titers also partitioned higher concentrations of such antibodies to the mammary glands. However, extreme variation in the concentration of specific colostral antibodies produced by animals has been noted.9,24 The present study evaluated antibody responses during the peripartum period in pregnant Holstein dairy cattle administered a multivalent killed virus vaccine according to label instructions.

In the present study, there were no adverse reactions such as anaphylactic shock, abortion, and stillbirth nor birth of weak unthrifty calves in the vaccinated group. Adverse reactions, especially abortion and to a lesser extent anaphylactic shock, have been reported when vaccines are first administered or multiple vaccines are given to pregnant cows in the prepartum period.12,25 The cattle in the present study had never been vaccinated with the multivalent killed virus vaccine product used. In fact, the study vaccine had never been used on this farm in any capacity, and the farm has been in existence for > 50 years. The study results have suggested there is less risk of adverse reactions following first-time administration of a multivalent killed virus vaccine product to improve colostrum quality, compared with the reported negative effects following first administration of a modified-live virus vaccine to naïve cows.12,25

One approach to the prevention of respiratory tract disease in calves is to increase the total amount of specific antibodies against BHV-1, BVDV type 1, and BVDV type 2 in the colostrum they receive, thereby facilitating improved antibody absorption by nursing calves. In the present study, the vaccine schedule used was a recommended standard protocol for administration of a multivalent killed virus vaccine to pregnant cattle. The response to vaccination was determined by assessment of titers of antibodies against BHV-1, BVDV type 1, and BVDV type 2 in both serum and colostrum obtained from vaccinated and unvaccinated cattle. The results indicated that titers of antibodies against BHV-1 and BVDV type 2 in the blood of vaccinated cows at approximately 5 weeks after their initial vaccine injection were significantly elevated, compared with those antibody titers in unvaccinated control cattle. A similar difference in SN antibody titers between groups was evident at the time of calving (approx 3 weeks after the booster vaccine dose had been administered). On the day of parturition (within 12 hours after calving), there were also significantly higher titers of antibodies against BHV-1 and BVDV type 2 in the colostrum of vaccinated cattle, compared with findings in unvaccinated cattle. The titer of antibodies against BVDV type 1 was also increased in the colostrum of vaccinates, compared with the titer in colostrum of controls, even though the titers of SN antibodies against BVDV type 1 were not significantly higher in the vaccinates, compared with findings for the unvaccinated cattle. These findings are in agreement with those of other studies5,18,h in which increased colostral antibody production against various pathogens was detected after vaccination of pregnant cattle during the immediate prepartum period. Higher titers of colostral antibodies against respiratory pathogens should, in turn, increase the rate of gastrointestinal antibody absorption, thereby protecting calves against respiratory tract disease early in life. With regard to anti–BHV-1 antibodies, calves naturally progress to seronegativity by approximately 170 days of age.22 For anti–BVDV antibodies, serum titers decrease to undetectable levels by 105 to 230 days of age.22,26,27

A surprising finding was that titers of SN antibodies against BVDV type 1 did not differ between the vaccinated and control groups. The initial titer of SN antibodies against BVDV type 1 measured 5 weeks after the first vaccine administration was the same in both groups (1:128). In unvaccinated cows at that time, the anti–BVDV type 1 antibody titer was twice that of the anti–BHV-1 or anti–BVDV type 2 antibody titer; therefore, it is possible that a wild strain of BVDV type 1 was introduced into this group of cattle. Commingling or fence line contact can lead to transmission of BVDV and BHV-1. It has been reported that in herds in which BVDV and BHV infections are endemic, serum antibody titers at any time prior to calving remain constant.28 On the farm of the present study, the routine immunization protocol required vaccination (with a multivalent modified-live virus vaccine) of cattle at 3 weeks after parturition. Research has shown that shedding of virus from animals vaccinated (according to label instructions) with a modified-live virus vaccine fails to result in detectable serum antibody titers in nonvaccinated pregnant cows with which those animals are in contact.29 Although it is possible that, when not lactating, some of the study cattle came into contact with recently vaccinated lactating cattle that were shedding the virus, it seems unlikely that the anti–BVDV type 1 antibody titers detected in the present study resulted from such contact. Nevertheless, given that vaccinated animals can become virus shedders and such shedding can interfere with the health of other animals and also with surveillance programs for known pathogens, it is critical to follow label directions when modified-live virus vaccines are used. The USDA gives exemptions for the use of modified-live virus vaccines in pregnant cows with the requirement that the vaccine is used in accordance with label directions.30 However, these possibilities do not explain the finding of a significant 3-fold increase in the titer of CN antibodies against BVDV type 1 in vaccinated versus unvaccinated cattle in the present study, when the titer of SN antibodies against BVDV type 1 in the vaccinated group was lower (albeit not significantly so) than that in the control group. The reason for the failure of the vaccine to elicit a robust SN anti–BVDV type 1 antibody response in the vaccinated cattle remains uncertain. There was a small but nonsignificant decrease (from 1:128 to 1:64) in SN anti–BVDV type 1 antibodies in vaccinated animals on the day of parturition, which probably represented translocation of serum antibody to the colostrum, even though a similar decrease was not observed in the control animals. The reason for this result is unknown but could certainly be beneficial to calves and warrants further investigation.

One potential shortcoming of the present study was that baseline SN antibody titers were not measured prior to the first treatment date. Although this information could have been useful, it is also possible that the results may have made interpretation more confusing because of the endemicity of these viruses in US cattle herds31,32 and the fact that the study farm maintained a regularly vaccinated herd. Even if the data were available, it would not be possible to distinguish between effects of natural exposure and those of the modified-live virus vaccine administered routinely on the farm.

Another potential problem in the present study was that differences in the age and parity between groups—a consequence of the presence of a greater number of heifers in the control group—could have biased the results. However, when within-group SN and CN antibody titer data for the young and older cattle were compared, the pattern of differences observed between young animals and older animals in both the control group and vaccinated group was the same, with the exception of titers of CN antibodies against BHV-1 in control animals, which were lower in younger cattle. Additionally, apart from the titers of SN antibodies against BVDV type 1, which were not significantly different between groups, all SN antibody titers were lower in control cattle than in vaccinated cattle, irrespective of age (Table 2). The median CN antibody titers against BVDV types 1 and 2 were all higher in vaccinates than in control cows but not significantly so in older animals, which may be better able to partition antibodies into colostrum at calving regardless of vaccination status. Nevertheless, we do not believe the disparity between age distributions in the 2 groups influenced the overall interpretation and conclusions of the study.

When available in abundance in colostrum, maternal antibodies that target respiratory tract pathogens and are able to be absorbed following ingestion are critical to calf protection. However, that antibody-derived protection is limited. Depending on the production of antibodies by dams and antibody uptake by calves, antibody protection could be negligible as early as 70 days of age.27,33 It has also been posited that maternal antibodies could even interfere with respiratory tract disease prevention programs that incorporate calf vaccination strategies.34 However, other evidence suggests that maternal antibodies may foster development of the calf's own immune response. Maternal antibodies might reduce but not eliminate viral replication, which in turn could allow the calf to develop an anamnestic response, resulting in innate antibody production.35 As a result, in calves with maternal antibodies, vaccination protocols that use modified-live virus vaccines should be helpful in prevention of respiratory tract disease, which lends support to the use of killed virus vaccines in nonlactating pregnant cattle to enhance production of CN antibodies and better protect calf health. On the basis of the results of the present study, provision of a multivalent killed virus stimulus to cattle during the prepartum period appeared to induce no adverse reactions and enhanced production of specific antibodies against known respiratory tract disease-causing pathogens; antibody titers in both serum (anti–BVDV type 2 and anti–BHV-1 antibodies) and colostrum (anti–BVDV type 1, anti–BVDV type 2, and anti–BHV-1 antibodies) were significantly increased following vaccination.

Acknowledgments

Presented in abstract form at the 26th World Buiatrics Congress, Santiago, Chile, November 2010.

None of the authors of this paper has a financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of the paper.

ABBREVIATIONS

BHV

Bovine herpesvirus

BRSV

Bovine respiratory syncytial virus

BVDV

Bovine viral diarrhea virus

CN

Colostrum neutralizing

IQR

Interquartile range (25th to 75th percentile)

SN

Serum neutralizing

Footnotes

a.

Bach A, Ahedo J, Kertz A. Using growth monitoring in heifer management and research (abstr). J Dairy Sci 2008;91:(suppl 1):602.

b.

Triangle 9 multivalent killed virus vaccine, Fort Dodge Animal Health, Fort Dodge, Iowa.

c.

Vacutainer, Fisher Scientific, Pittsburgh, Pa.

d.

Zoetis, Lincoln, Neb.

e.

SAS, version 9.2, SAS Institute Inc, Cary, NC.

f.

STATA, version 13.1, StataCorp, College Station, Tex.

g.

DairyComp 305, Valley Agricultural Software, Tulare, Calif.

h.

Stegner J, Alaniz G, Meinert T, et al. Passive transfer of antibodies in pregnant cattle following vaccination with Bovi-Shield (abstr), in Proceedings. Annu Meet Am Assoc Bovine Pract 2010;250.

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Contributor Notes

Address correspondence to Dr. Smith (bis@vet.upenn.edu).