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ANIMAL GENETICS |
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* University of Florida, Institute of Food and Agricultural Sciences, Range Cattle Research and Education Center, Ona 33865;
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Subtropical Agricultural Research Station, USDA, ARS, Brooksville, FL 34601;
and
Grazinglands Research Laboratory, USDA, ARS, El Reno, OK 73036; and
Department of Animal Sciences, University of Florida, Gainesville 32611
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Abstract |
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 Top Abstract INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Key Words: acute phase protein • beef cattle • Brahman • crossbreeding • Romosinuano • stress response
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INTRODUCTION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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). Measurement of plasma acute phase proteins has been demonstrated to be an indicator of stress in weaned, transported calves (Arthington et al., 2003a; 2005).
A population of purebred and crossbred Brahman, Angus, and a Criollo breed, the Romosinuano, was created to estimate genetic effects in Florida (Riley et al., 2007). This population offered diverse backgrounds and sources of adaptation to the rigorous conditions of the tropics and subtropics; these cattle also may vary in their responses to the stressors associated with weaning and transportation. Limited research has attempted to estimate genetic effects for concentrations of circulating hormones in livestock (Van Mourik et al., 1986; Hammond et al., 1996; Odeh et al., 2003), and apparently no studies have attempted to estimate genetic effects for acute phase proteins.
The objective of this study was to estimate genetic effects, including heterosis and breed direct and maternal effects, in Romosinuano, Brahman, and Angus calves and crosses of these breeds on the acute phase protein response to 2 stressors: weaning and long-distance transportation 28 d after weaning.
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MATERIALS AND METHODS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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All procedures involving animals were approved by the local institutional animal care and use committee.
Calves were produced in a project to evaluate the Criollo breed Romosinuano at the Subtropical Agricultural Research Station in Central Florida. The overall project breeding design was detailed previously (Riley et al., 2007). Resultant purebred and crossbred calves were spring-born from 2002 through 2004. Calves were identified at birth, and males were castrated at that time. Calves (n = 1,032) were weaned at approximately 7 mo of age in September of each year in 3 separate weeks (3 separate locations; cow breeds and breed combinations of calves were balanced across these STARS locations). A total of 12, 11, and 15 Angus, Brahman, and Romosinuano bulls sired progeny with records (average of 28, 32, and 23 calves per Angus, Brahman, and Romosinuano sire, respectively). Weaned calves were provided a commercial preconditioning concentrate (medicated; 14% CP as-fed, cottonseed/soybean meal-based ration; 1.8 kg per calf per day) for 21 d and free-choice grass hay. Approximately 28 d after weaning, the steers (n = 482) were transported 1,800 km to the USDA-ARS Grazinglands Research Laboratory at El Reno, Oklahoma.
Traits Evaluated
Blood samples from steer and heifer calves were collected from the jugular vein into Li-Heparin LH (/9 mL) tubes (Sarstedt Inc., Newton, NC) at weaning and at 24 and 72 h after weaning. Additional blood samples were collected from steers transported to Oklahoma immediately before shipment, upon arrival, and at 24 and 72 h after arrival. Tubes were placed on ice until plasma could be collected. Plasma was collected by centrifuging the blood at 2,000 x g for 20 min and stored at –20°C for later analysis. Plasma concentrations of 3 acute phase proteins were assayed, including haptoglobin, ceruloplasmin, and fibrinogen. Both steers and heifers were sampled at weaning and at 24 and 72 h after weaning. Most of these same steers were transported to Oklahoma. These steers were sampled immediately before shipment and on arrival in Oklahoma, and again at 24 and 72 h after arrival.
Plasma haptoglobin concentrations were determined in duplicate samples by measuring haptoglobin/hemoglobin complexing by the estimation of differences in peroxidase activity (Makimura and Suzuki, 1982). Results are expressed as arbitrary units resulting from the absorption reading at 450 nm x 100. For samples with an absorption reading 
0.010, the intraassay CV of duplicate samples was controlled to values 20%, and for samples with an absorption reading 
0.010, the intraassay CV of duplicate samples was controlled to values 10%.
Plasma ceruloplasmin oxidase activity was measured in duplicate samples using colorimetric procedures described by Demetriou et al. (1974). The intraassay CV of duplicate samples was controlled to values 5%. Ceruloplasmin concentrations were expressed as milligrams per deciliter, as described by King (1965).
Plasma fibrinogen concentrations were determined using a fibrinogen determination kit (Sigma procedure No. 880; Sigma Diagnostics, St. Louis, MO). The intraassay CV was controlled to values 5%.
Interassay variation of acute phase proteins were controlled to CV limits 10%, as a result of a standard pooled sample analyzed in duplicate within each individual assay run. When the interassay CV exceeded 10% for all runs within an assay, all samples contained in the individual run with the standard pool exceeding the average by the greatest amount were reanalyzed. This step was repeated until the results of standard pools for all runs resulted in a CV 10%.
Statistical Analysis
Data were analyzed using mixed linear models with the MIXED procedure (SAS Inst. Inc., Cary, NC). Data were grouped into 2 sets: 1) calves at weaning, and 2) steers at shipment. Separate analyses were conducted; data from the 2 (samples at weaning from both sexes vs. samples from steers when transported) were never combined. All of the steers with records in the second data set also had records in the weaning data set; however, these data were analyzed separately. Fixed effects included sire breed, dam breed, sampling time, birth location, calf sex (weaning data only), year of record, cow age in years, and interactions. Interactions of special interest included sire breed x dam breed, because it indicates calf breed, and the 3-way interaction of sire and dam breed with sampling time. Age of calf in days at weaning and BW at weaning were investigated as linear and quadratic covariates. Sire of calf within sire breed was a random term in all models. The fixed effect portion of each model was determined while using a simple correlation structure for repeated measures (compound symmetry).
For each trait, the fixed portion was subsequently held constant and the covariance between repeated sampling times within each analysis (weaning or steers at shipment) was modeled, investigating various structures for each trait using the procedures described by Littell et al. (2002). These investigated structures included 1) a single residual variance, 2) compound symmetry (equal variances for each sampling time and equal covariances among all pairs of sampling times, resulting in estimation of 2 covariances), 3) heterogeneous compound symmetry (unequal variances for sampling times and unequal covariances between pairs of sampling times, consisting of estimates of 4 covariances for the weaning data set and 5 for the shipment data set), and 4) first order antedependence structure (permitting unequal sampling time variances and unequal correlations between sampling times, resulting in 6 and 8 covariances estimated for the weaning and shipment data sets, respectively). Information criterion values generated by the MIXED procedure were considered in the determination of best residual covariance structure for each trait; however, priority was given to Schwarz’ Bayesian information criterion values because of the stringent penalty applied to this criterion value for the number of parameters estimated. After a covariance structure was selected that best modeled the correlation between repeated measures, the significance of fixed effects was confirmed with that structure.
Least squares means (and differences among least squares means) for acute phase protein concentrations of breed groups and breed group x sampling time interactions were of interest. There were an excessively large number of possible comparisons of these concentrations. Pairwise differences were assessed using t-tests with a Bonferroni adjustment to guard against the chances of erroneously detecting significant differences.
Contrasts of appropriate least squares concentrations were constructed based on principles described by Dickerson (1973) to estimate breed maternal, breed direct, and heterosis effects for each trait. Maternal breed effects were estimated as the average difference between reciprocal crossbred groups; e.g., the Romosinuano maternal effect is 
[(AR – RA) + (BR – RB)], and pairs of letters indicate calf breed group concentrations in which the first and second letters indicate the breed of sire and dam of calves in the group; and R, B, and A indicate Romosinuano, Brahman, and Angus, respectively. Direct breed effects for each breed were estimated as the purebred mean minus the maternal effect for that breed minus the average of the other 2 pure breeds; e.g., Romosinuano is RR – [(AR – RA) + (BR – RB)] – [(AA+ BB)]. Within a trait, the estimates of breed direct or maternal effects sum to 0. Estimates of heterosis for pairs of breeds for each trait consisted of a contrast between the averages of the crossbred and purebred groups; e.g., the heterosis for Romosinuano and Brahman is [(RB + BR) – (RR + BB)].
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RESULTS AND DISCUSSION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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All information criterion values, including Schwarz’ Bayesian information criterion values, favored a heterogeneous compound symmetry structure for modeling the variance and covariance associated with repeated measures for ceruloplasmin and fibrinogen. These variance estimates (unique for each sampling time) and estimates of correlation among sampling times are presented in Table 1. The simpler compound symmetry structure was favored for the haptoglobin model, in which the estimated variance was the same for all sampling times (Table 1). In the haptoglobin model, the single estimate of covariance resulted in a very low correlation (r = 0.07) among repeated measures associated with sampling times.
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. Cow age did not affect any of the 3 acute phase proteins in calves at weaning (P > 0.29). Regression of these traits on weaning age or BW was never important (P > 0.4). Year of record was highly significant for all acute phase proteins. Heifers had greater (P < 0.001) plasma ceruloplasmin concentrations than steers (Table 3), but calf sex was not important (P > 0.31) for haptoglobin or fibrinogen concentrations. Linear regression coefficients of ceruloplasmin and fibrinogen concentrations on calf age were 0.02 ± 0.004 and 0.25 ± 0.06 mg/dL, respectively (P < 0.001), but calf age was not retained in the final haptoglobin model (P = 0.4). Birth location was highly significant for ceruloplasmin and fibrinogen, and was important (P = 0.07) for haptoglobin concentrations. Plasma haptoglobin concentrations at 72 h were significantly greater (P < 0.05) than concentrations at weaning and 24 h after weaning (Table 3). Fibrinogen concentrations increased from 0 to 72 h postweaning; all concentrations significantly differed from each other (Table 3). Noteworthy here is the relatively quick response in fibrinogen concentration following weaning, that is to say, the immediate separation of calves from their dams or the procedures themselves, which included restraint and bleeding. Even though the increase in haptoglobin concentrations occurred later, the magnitude of the increase was much greater than for fibrinogen concentrations. This difference is likely due to the unique character of haptoglobin. Unlike fibrinogen and ceruloplasmin, which exist at basal levels in unstressed cattle, haptoglobin concentrations are virtually undetectable in the blood of nonstressed calves (Makimura and Suzuki, 1982).
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). The F1 Romosinuano-Angus and Brahman-Angus calves had significantly greater fibrinogen concentrations than purebred Brahman and Romosinuano-sired calves out of Brahman dams.
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). In all other breed groups (except F1 calves with Angus sires and Brahman dams) 72 h postweaning concentrations were significantly greater than concentrations at 0 and 24 h postweaning. There were some breed group concentration differences at 72 h postweaning; purebred Angus were significantly lower than purebred Romosinuano. Although not significantly different than all breed groups, calves with Angus sires had the lowest ceruloplasmin concentrations within different sampling times.
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Information criterion values favored first order ante-dependence structures for sampling times of haptoglobin and ceruloplasmin. The variance estimate for haptoglobin concentrations 24 h after arrival in Oklahoma was over 3 times as large as any other sampling time variance (Table 6). In the analysis of haptoglobin, residual correlations of sampling times were 0.26 or smaller (Table 6). The largest variance estimate for ceruloplasmin was at arrival after transportation, and the correlation estimates among sampling times were generally large and positive. A compound symmetry structure was favored for fibrinogen models.
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). Cow age was not retained in any final model (P > 0.51), nor was any regression of acute phase protein concentrations on steer age or BW (P > 0.72). Sampling time was a highly significant main effect on haptoglobin and fibrinogen concentrations. Transportation dramatically influenced plasma concentrations of these acute phase proteins; they were least at shipment (Table 3), and both were significantly greater upon arrival. Haptoglobin increased greatly; the mean at 24 h after arrival was 288% of the mean at shipment (Table 3). Fibrinogen concentrations also increased with sampling time, but by a smaller amount (6% from shipment to arrival), and the fibrinogen mean at 24 h after arrival did not differ (P > 0.05) from the arrival mean, and was 13% greater than the shipment mean 72 h after arrival.
The influence of sire and dam breed varied for the response patterns of the acute phase proteins in transported steers. No main or interaction effects for sire or dam breed were retained in the analyses of haptoglobin (P > 0.41). The interaction of sire breed and dam breed (P = 0.016) in fibrinogen analyses was supported by the high concentrations for steers sired by Romosinuano and out of Angus dams (Table 4). These were significantly greater than concentrations for purebred Romosinuano and Brahman, and reciprocal Romosinuano-Brahman steers.
There appeared to be differential breed acute phase protein responses to transportation stress, supported by the significant interaction of sire breed, dam breed, and sampling time in the analysis of ceruloplasmin concentrations in transported steers. In general, cerulo-plasmin concentrations at shipment were the least for all breed groups; however, this result was not significant for all breed groups (Table 7). Ceruloplasmin concentrations were greater (P < 0.05) upon arrival than at shipment for all breed groups except those that had Angus sires. Ceruloplasmin concentrations in purebred Angus calves did not differ (P > 0.05) among any of the collection times. In contrast, ceruloplasmin concentrations in purebred Romosinuano calves differed among all 4 sampling times. In general, ceruloplasmin concentrations were lower in sampling times after arrival for all breed groups. Ceruloplasmin concentrations at 24 h after arrival were not significantly different from those at arrival for any breed group other than purebred Romosinuano. Concentrations at 72 h after arrival were significantly lower than those at arrival for purebred Romosinuano and all breed groups with Brahman sires. The only detected breed difference within a sampling time was the larger (P < 0.05) ceruloplasmin concentration for purebred Romosinuano steers as compared with Angus steers upon arrival.
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A large estimate of heterosis (44% of purebred average) was detected for Brahman-Angus haptoglobin concentrations at weaning (Table 8). Estimates of Romosinuano-Angus heterosis were significant for fibrinogen concentrations in calves at weaning (10.3%) and in steers at shipment (20.1%). These are greater than many heterosis estimates for production traits in cattle (Long, 1980; Wyatt and Franke, 1986). This is not the first detection of an apparent nonadditive genetic influence on circulating concentrations of stress-related products in blood, as Van Mourik et al. (1986) detected considerable heterosis (86%) for stress-response plasma corticosterone concentrations in chickens. However, others have failed to detect such heterosis in cattle (Hammond et al., 1996) or in quail (Odeh et al., 2003). Beyond confirming that it exists, we are unable to suggest that the detected heterosis is beneficial, because as of yet, it is really unknown which (high or low) circulating levels of these proteins are desirable. In this experiment, measures of growth performance among the F1 cattle have excelled in the preliminary analyses (unpublished data).
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). Significant direct effects on ceruloplasmin concentrations were detected for Romosinuano of approximately the same magnitude in the weaned calf and transported steer analyses (Table 8). Angus direct effects on ceruloplasmin concentrations in weaned calves were negative. Significant Angus maternal effects were positive for ceruloplasmin concentrations in weaned calves and approached significance for fibrinogen concentrations in weaned calves (P = 0.074) and in transported steers (P = 0.12). Negative maternal effects were detected in Romosinuano for ceruloplasmin concentrations (P = 0.006). Odeh et al. (2003) reported strong maternal effects on plasma corticosterone concentrations in response to restraint stress in quail. It was unexpected that the negative Brahman maternal effects on fibrinogen concentrations in weaned calves and the Brahman-Angus heterosis for haptoglobin concentrations in weaned calves were the only Brahman effects detected in these analyses; Phillips et al. (1989) detected higher fibrinogen concentrations during weaning and transit for Bos indicus (half blood) calves compared with Bos taurus calves. Brahman effects, both direct and maternal, on a variety of traits frequently are extreme or opposite in sign from those of Bos taurus breeds simultaneously evaluated (Wyatt and Franke, 1986; Prayaga, 2004; Riley et al., 2007). Breed-Related Characteristics of Acute Phase Proteins and Potential Application to Beef Production
A long-term aim of our research efforts, of which this study is a part, is to attempt to assess the utility of using acute phase protein concentrations to predict postweaning calf performance. Although there is evidence that acute phase protein concentrations are elevated in morbid feedlot cattle (Carter et al., 2002; Berry et al., 2004), there has been little effort placed on linking acute phase protein concentrations to the performance of apparently healthy calves. One of several potential factors that may influence this effort is genetic-related differences in acute phase protein responses to stress. The results of the current study provide the first information relative to this issue because it appears that breed differences do indeed exist. Weaned and transported calves with Angus sires generally had the least ceruloplasmin concentrations at the various sampling times. This characteristic was evident before and after the stress induction (weaning and transportation). Breed differences, relative to ceruloplasmin, are not necessarily dependent solely upon stress. Ceruloplasmin is a Cu-dependent protein and represents as much as 95% of the total Cu found in blood (Cousins, 1985). Concentrations of ceruloplasmin are dependent on the overall Cu status of cattle and are reflective of the Cu content of the diet (Arthington et al., 1996). Despite being provided access to similar sources of forage, water, and mineral supplement, variation in Cu metabolism among different breeds of beef cattle is apparent (Ward et al., 1995). Potential differences in Cu metabolism, as well as responsiveness to management stress (weaning and transport), must be considered when evaluating differences in ceruloplasmin concentrations among beef breeds. In the current study, plasma cerulo-plasmin concentrations of Angus-sired calves appeared to be less responsive to the stressors of weaning and transportation than those of other breed groups. It is not necessarily appropriate to conclude that these calves were under a lower amount of stress; indeed, differences in how these calves metabolize Cu may be a more influential factor. This stated, there is also evidence that breed differences exist relative to response to the stressors associated with transportation (Blecha et al., 1984; Phillips, 1984). The design of the current study was not constructed to directly separate the response variables associated with Cu metabolism and stress; however, it is interesting to note that of the acute phase proteins measured in this study, ceruloplasmin revealed the greatest Pearson correlation coefficient when analyzed against 30-d ADG of calves following transportation. Animal performance results associated with this study are being compiled in a separate manuscript; however, in the current study it is meaningful to note that simple correlations of 72-h ceruloplasmin concentrations with 30-d ADG were significant for all breed combinations except Angus-sired calves (P < 0.08; average r = –0.31). These potential breed differences relative to the responsiveness of ceruloplasmin to stress may also impact fibrinogen because Cu-deficient cattle with reduced ceruloplasmin concentrations have greater fibrinogen concentrations following stress induction compared with Cu-adequate cattle (Arthington et al., 1996, 2003b). In the current study, the increased concentrations of fibrinogen (postweaning) in calves from Angus dams may be related to this fibrinogen-ceruloplasmin association. It is commonly recognized that acute phase proteins are released into the blood following stimulation by 1 of 3 proinflammatory cytokines (IL-1, IL-6, and TNF-
Baumann and Gauldie, 1994). Although we are unclear which specific cytokine stimulates each acute phase protein in cattle, a link between Cu nutrition and these proinflammatory cytokines has been reported (Lukasewycz and Prohaska, 1990; Gengelbach and Spears, 1998). Additional research is needed to determine if plasma acute phase protein concentrations may be used as an indicator of subsequent performance of calves. Data of the current study imply that breed differences do exist among acute phase protein concentrations of stressed calves, and consideration of these breed-associated differences will likely impact subsequent efforts to link acute phase proteins to performance of stressed calves.
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Footnotes |
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2 Appreciation is extended to E. L. Adams, E. J. Bowers, M. L. Rooks, V. E. Rooks, and all of the STARS staff for technical assistance and animal care.
3 Present address: Land O’Lakes (Beijing), Room 705, Office Tower 1, Henderson Centre, Tower 1, 18 Jian Guo Men Nei Ave., Beijing 100005, China.
4 Corresponding author: David.Riley{at}ars.usda.gov
Received for publication December 27, 2006. Accepted for publication May 31, 2007.
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LITERATURE CITED |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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