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Ontario Veterinary College, University of Guelph, Guelph, Ontario N1G 2W1, Canada
1 Corresponding author: keleslie{at}uoguelph.ca
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Key Words: calf • failure of passive transfer • maternal immunity • risk factor
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Passive transfer of immunity in calves may be assessed by several methods, including direct measurement of serum IgG by ELISA or radial immunodiffusion (Filteau et al., 2003) and estimation of serum IgG concentration by measuring serum total protein (TP) by refractometry (Wallace et al., 2006). The latter method has been reported to be a reliable screening test for the assessment of passive transfer in calves, with a sensitivity and specificity of greater than 80%, when test end points of 5.0 or 5.2 g/dL are used for diagnosis of failure of passive transfer (FPT; Calloway et al., 2002).
To date, several reports have been published on factors associated with the acquisition of passive immunity in newborn calves in the United States (Besser et al., 1991; Perino et al., 1995; Quigley et al., 2001) and in Quebec, Canada (Filteau et al., 2003). However, there is a lack of published information of this kind in relation to dairy calves in Ontario, Canada. Such information is important to determine whether additional measures need to be taken by the industry to ensure adequate transfer of passive immunity to calves entering the dairy and veal industries, and to investigate whether calf management practices prevalent in the province may have an effect on the risk of FPT. Furthermore, there is concern that calves entering the veal industry from dairy farms may not be receiving adequate quantities of colostrum and, as a result, may suffer from greater rates of FPT than replacement dairy heifers. Therefore, in the work reported here, data collected on southern Ontario dairy farms during 2 large dairy calf health studies conducted in 2003 and 2004 were analyzed to assess passive immunity in calves up to 8 d of age on southern Ontario dairy farms. In addition, these data were investigated to determine whether the level of acquisition of passive immunity in these calves was associated with colostrum feeding methods and other calf management practices.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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The second study (referred to hereafter as the herd-level study) was carried out from May to October 2004 on 119 dairy farms throughout southern Ontario (Trotz-Williams et al., 2007b). That study was conducted with the objective of investigating associations between farm management practices and the within-herd prevalence of C. parvum. Herds of various sizes, and representing several management styles, were included in the study. The number of milking cows per farm ranged from 17 to 950, with a mean of 95 cows and a median of 70. On most farms, all cows were Canadian Holsteins. In addition to collection of fecal samples for testing for Cryptosporidium, jugular blood samples were drawn in plain 10-mL Vacutainer tubes (Becton Dickinson and Company) from a maximum of 5 calves on each farm, up to and including 7 d of age. A questionnaire was administered on each farm to gather information on farm-level management practices. As in the first study, this questionnaire included questions on colostrum storage and feeding methods used on the farms. However, information collected in this work referred only to herd-level practices to which individual calves had been exposed. Questionnaires from both studies are available from the authors in English.
In each study, blood samples were placed in a cooler immediately after collection and transferred to a refrigerator for storage for up to 24 h. Sera were separated from blood samples within 24 h. Serum refractometry was performed by using a handheld refractometer (SPR-Ne, Atago Company, Kirkland, WA), in accordance with the manufacturers’ instructions, to determine serum TP content as a measure of passive transfer of maternal immunity. A test end point (cutoff value) of 5.2 g/dL was used; that is, FPT was defined as serum TP concentrations of <5.2 g/dL (Calloway et al., 2002).
Statistical Analysis
Data were entered into EpiData and Microsoft Access databases and exported into Stata 9.0 (StataCorp LP, College Station, TX) for statistical analysis.
Calf-Level Study.
For data from this study, descriptive analyses were carried out to determine the distribution of serum TP levels among the calves, as well as the number of calves exposed to each management practice to be investigated for associations with TP levels and the risk of FPT. For the purposes of this work, FPT was defined as serum TP concentrations below 5.2 g/dL (Calloway et al., 2002). Mixed effects linear regression was then used to investigate the data collected in this study for any association between serum TP (as a continuous outcome or dependent variable) and sex of the calves (as the independent variable). Mixed effects logistic regression was used to explore the data for any significant association between FPT (as a dichotomous outcome variable) and sex of the calves (as the independent variable). Each model included farm as a random effect to control for any effect of clustering of data within herds. Model diagnostics were performed by generating and examining residuals and expected values (probabilities) of the outcome (Dohoo et al., 2003). Because colostrum-feeding practices were largely at the herd level, and only a small number of farms were represented in the data (n = 11), no analyses were undertaken for associations between calf management variables and serum TP levels or FPT.
Herd-Level Study.
For these data, descriptive analyses were carried out to determine the distribution of serum TP levels among the calves, as well as the number of farms using each management practice to be investigated for associations with TP levels and the risk of FPT. As for the calf-level data, FPT was defined as serum TP concentrations below 5.2 g/dL (Calloway et al., 2002). Mixed effects linear regression was then used to investigate the data for any association between serum TP (as a continuous outcome variable) and sex of calves (as the independent variable). In addition, mixed effects logistic regression was used to explore the data for any association between FPT (as a dichotomous outcome variable) and sex of the calves (as the independent variable). Each mixed model included farm as a random effect to control for the effect of clustering within herds. The same regression methods were used to model management variables (as independent variables) on serum TP (as a continuous outcome variable using linear regression) or FPT (as a dichotomous outcome variable using logistic regression) to look for statistically significant associations. Here again, each model included farm as a random effect to control for the effect of clustering within herds. Associations were examined first by using univariable models, and subsequently by constructing multivariable models that included independent variables that were statistically significant in univariable models. Final multivariable models were produced by using the manual backward elimination procedure described by Dohoo et al. (2003), with a significance level of P > 0.05 as the criterion for removal of a variable from the model. Model diagnostics were performed by generating and examining residuals and expected values (probabilities) of the outcome (Dohoo et al., 2003).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Data from the Calf-Level Study
Description of Calves.
Of the 961 calves in this study, 606 (63.1%) were born in the warmer months (June to October 2003) and 355 (36.9%) were born in the following winter (January to April 2004). Information on sex was recorded for 932 of the 961 calves: 355 (38.1%) were male (bull) calves, 575 (61.7%) were females (heifers), and 2 calves (0.2%) were freemartins. Twenty-eight (2.9%) of the 961 calves were less than 1 d of age at sampling.
Maternal Immunity and FPT.
A highly significant difference (P < 0.001) was found between the mean serum TP levels of calves less than 1 d of age (5.4 g/dL) and those of calves 1 d of age and older (6.3 g/dL). Therefore, calves less than 1 d of age were omitted from all analyses that included serum TP or FPT as an outcome variable. Serum TP measurements for the calves 1 d of age or older (n = 933) ranged from 3.5 to 8.6 g/dL (average 6.3 g/dL; median 6.3 g/dL) and are summarized in Figure 1
. Using a cutoff value (test end point) for FPT of 5.2 g/dL, 78 (8.4%) of the 933 calves showed serum TP levels indicative of FPT.
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Colostrum Feeding Practices.
Calf management (including colostrum feeding) methods to which calves were exposed are summarized in Table 1. Where information on management methods was missing, calves were excluded from counts; therefore, total counts for some variables are less than 961 calves.
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, although approximately equal proportions (between 20 and 30%) of the calves in the study were born in each of the four 6-h periods of the day or night, fewer than 50% of the calves were allowed to remain with their mothers for more than 1 h after birth. The calf’s mother was reported as the most common source of colostrum given to the calves, with 59.4% of calves receiving colostrum from their mothers. Pooled colostrum was given to 45.5% of the calves in the study. Most (75.4%) of the calves received fresh colostrum, whereas 55.0% were given colostrum that had been frozen. Most (89.0%) of the calves were bottle-fed colostrum; however, 30.9% were tube-fed. In fact, 202 calves received colostrum both by bottle and by tube (not shown in Table 1). The amount of colostrum given in each interval of time within the first 24 h of birth varied from 0 to 4 L for the first 6 h, 0 to 6 L for the next 6 h, and 0 to 9 L for the last 12 h (12 to 24 h after birth). In each period, the most commonly stated quantity of colostrum given was 2 L (not shown in Table 1). Information on the number of feedings represented by these volumes was not collected in the study and is therefore not presented in the table.
Data from the Herd-Level Study
Description of Calves.
Serum TP refractometry readings were available for 423 calves on 112 of the 119 farms in this study. Serum TP concentrations were not measured in calves from the remaining 7 farms; therefore, these were excluded from the analysis. Because recording of the sex of the calves was not relevant to the objectives of the original study, this was done only for some calves. As a result, data on sex were available for only 244 calves from 65 farms. Of these 244 animals, 119 (48.8%) were males (bull calves) and 125 (51.2%) were females (heifers). The ages of 421 calves were known: these ranged from a few hours (<1 d) to 7 d of age. Sixteen calves (3.8%) were less than 1 d of age at the time of testing.
Maternal Immunity and FPT.
Serum TP measurements for all calves in this data set ranged from 3.2 to 9.8 g/dL, with an average of 5.4 g/dL and a median of 5.4 g/dL. Serum TP measurements for calves 1 d of age and older also ranged from 3.2 to 9.8 g/dL, with an average of 5.4 g/dL and a median of 5.4 g/dL. For calves in this data set, no significant difference (P = 0.944) was found between the mean serum TP levels of calves <1 d of age (5.4 g/dL) and those of calves 1 d of age and older (5.4 g/dL). Nevertheless, for consistency of approach, calves under 1 d of age were omitted from all regression analyses that included serum TP or FPT as an outcome (dependent) variable. Serum TP levels for calves 1 to 7 d of age (n = 407) are summarized in Figure 2. Within-herd median values ranged from 4.2 to 7.0 g/dL, with an average of 5.4 g/dL. Results for 151 calves (37.1%) indicated FPT (serum TP levels <5.2 g/dL).
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Colostrum Feeding Practices.
Table 2 summarizes the calf management and colostrum feeding practices used on the dairy farms participating in the herd-level study. As in the calf-level study, information was not collected on the number of feedings represented by the quantities of colostrum reported by producers. Where information on management methods was missing, calves or farms were excluded from counts. Therefore, total counts for some variables was less than 423 calves or 112 farms.
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). No other calf management variables were significantly associated with serum TP concentrations.
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). The percentage of calves on a farm that were allowed to suckle colostrum directly from their dams, as reported by producers, was also significantly and positively associated with an increased risk of FPT. In other words, calves on farms where a greater percentage of calves were reportedly allowed to suckle from their dams had increased odds of FPT compared with calves on farms where a lower percentage of calves were allowed to suckle. On the other hand, the quantity of colostrum that producers reported giving to calves in the first 6 h after birth was significantly, and negatively, associated with the risk of FPT: the greater the quantities of colostrum that producers reported giving in the first 6 h after birth, the lower the odds of FPT in their calves. No other management variables were significantly associated with the risk of FPT (P > 0.05).
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. No interactions or confounding was evident during the construction of this model, and examination of residuals and predicted probabilities indicated good model fit.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Analyses of the data with serum TP as the dependent variable yielded different results from those obtained when FPT was used as the dependent variable. Although one of these variables (FPT) is derived from the other (serum TP), they are in fact quite different in nature so that trends seen for the continuous form of the variable may not be apparent when that variable is dichotomized as FPT, and vice versa. Because FPT, rather than serum TP, is known to be associated with calf health outcomes (Robison et al., 1988; Virtala et al., 1999), this may be considered the more useful dependent variable in these analyses. As such, the analyses performed when using serum TP as an outcome provided information that is of use more for research purposes than for practical application. This considered, the proportion of calves showing FPT was much greater (37.1%) in calves in the herd-level study than in calves in the calf-level study (8.4%). Because of the large number of farms included in the herd-level study, the greater estimate of prevalence of FPT was less likely to have been influenced by individual farms and more likely to be representative of southern Ontario dairy herds in general. Having said this, a FPT prevalence estimate of more than 30% implies that, on dairy farms within the study area, increased efforts need to be applied to ensure the adequate transfer of maternal immunity to newborn calves.
The results reported here also provide useful data on the methods used on Ontario dairy farms for the storage and feeding of colostrum (Tables 1 and 2). Because farms in the described studies represented a wide spectrum of herd size and management practices, data obtained from these farms were also likely to give a representative overview of calf management practices used by southern Ontario dairy producers.
Most of the predictors used in assessing risk factors for FPT were measured at the herd level, whereas outcomes (serum TP and FPT) were recorded at the calf level. It is therefore possible that the responses recorded for each farm in the study did not apply to all individual calves on that farm. For this reason, factors found to be significantly associated would best be further examined in a future study to verify the existence of such associations. Nevertheless, the variables that were shown here to be associated with passive transfer outcomes all offer biologically plausible explanations for the statistical associations. As such, we believe that these are potentially true predictors of these outcomes in dairy calves in southern Ontario.
The results shown in Tables 4 and 5 indicate that the odds of FPT in calves on farms where producers reported that calves were usually left with their dams for 3 h or more after birth were nearly twice the odds of FPT as in calves on farms where dams and calves were usually separated within 3 h of birth. This finding appeared to be supported by the fact that the producer-estimated percentage of calves allowed to suckle colostrum directly from their dams also showed a significant and positive association with the risk of FPT in calves. Not surprisingly, these 2 variables were moderately and positively correlated with each other (correlation coefficient 0.22). On the other hand, the amount of colostrum that producers reported giving to calves within the first 6 h of birth showed a significant negative association with the risk of FPT in calves. This variable was moderately and negatively correlated with the former 2 variables (correlation coefficients –0.15 with length of time with the dam and –0.23 with percentage receiving colostrum from the dam). These results would seem to indicate that, as mentioned in other published reports (Besser et al., 1991), calves allowed to remain with and suckle from their dams for more than 3 h after birth are less likely to receive sufficient colostrum in the first 6 h, and are therefore more likely to develop FPT. Furthermore, calves on farms where the practice is to separate dams and calves as soon as possible after birth are more likely to receive known quantities of colostrum by other means (e.g., bottle or esophageal tube) so that adequate intake of colostrum is more ensured and FPT is less likely (Filteau et al., 2003).
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Received for publication November 27, 2007. Accepted for publication May 23, 2008.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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