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Effect of transportation and commingling on the acute-phase protein response, growth, and feed intake of newly weaned beef calves¹

J. D. Arthington^*,2, S. D. Eicher, W. E. Kunkle and F. G. Martin

^* University of Florida-IFAS, Range Cattle Research and Education Center, Ona; and Department of Animal Sciences, Gainesville; and and Department of Statistics, Gainesville; and and USDA, ARS, West Lafayette, IN

² Correspondence:
3401 Experiment Station, Ona, 33865 (phone: 863-735-1314; fax: 863-735-1930; E-mail:
jdarthington{at}mail.ifas.ufl.edu).

	Abstract

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The objective of this study was to investigate the effect of transportation and commingling on measures of the acute-phase protein response in newly weaned beef calves. Thirty-two (Exp. 1; average BW = 266 ± 20.8 kg) and thirty-six (Exp. 2; average BW = 222 ± 34.6 kg) Brahman-crossbred calves were randomly allotted to one of four treatments (2 x 2 factorial arrangement [transportation x commingling] in a completely randomized design). Body weight and jugular blood were collected at weaning, after shipment, and 1, 3, and 7 d after transport for Exp. 1, and at weaning and 1, 5, 9, 13, 17, and 21 d after transport for Exp. 2. Feed intake within pen was recorded daily for Exp. 2. Plasma fibrinogen, ceruloplasmin, haptoglobin, and cortisol concentrations were determined for all collection times. Additionally, serum amyloid-A and -acid glycoprotein concentrations were determined in Exp. 1 and 2, respectively. In Exp. 2, commingled calves tended (P = 0.13) to have a higher DMI than noncommingled calves (5.3 and 4.8 kg/d, respectively). Transported calves lost more BW than nontransported calves from the time of weaning to d 1 (2.0 and 3.1% more BW loss for Exp. 1 and 2, respectively). With the exception of haptoglobin in Exp. 1, each of the acute-phase proteins measured in these studies increased over each sampling day. In Exp. 1, transported calves had higher (P < 0.05) mean serum amyloid-A concentrations than nontransported calves (48.9 vs. 33.4 µg/mL). There was a significant sampling day x transportation interaction (P < 0.01) for fibrinogen, ceruloplasmin, and haptoglobin in Exp. 1; transported calves had higher concentrations of fibrinogen following transport and on d 2 and 3, and ceruloplasmin on d 3. Haptoglobin concentrations were higher (P = 0.04) in nontransported calves on d 1 and 2 of Exp. 1. In Exp. 2, overall mean haptoglobin concentrations were higher in nontransported vs. transported calves. The results of these studies indicate that stressors associated with transportation affect the acute-phase protein response in newly weaned beef calves. More research is needed to determine whether these proteins might be valuable indicators of stress following the weaning process.

Key Words: Acute-Phase Proteins • Calves • Mixing • Transport

	Introduction

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Cattle undergo a variety of stressors within normal production processes. In general, these stressors may be grouped into two broad categories: 1) psychological stress, such as commingling, restraint, and novel exposure, and 2) physical stress, such as hunger, injury, disease, and environmental pressure (Grandin, 1997). One of the most widely recognized stressors in beef cattle production is transportation. In weaned feeder calves, transportation stress has been shown to increase blood neutrophil number and decrease lymphocyte responsiveness to mitogen stimulation (Blecha et al., 1984) and increase serum cortisol concentration (Crookshank et al., 1979).

An occurrence of stress may be defined in many ways; in general, it is described as any challenge that disrupts the animal’s internal environment (Sheridan et al., 1994). This may or may not result in clinical disease. The animal’s ability to readily respond and adapt to stress stimuli likely influences the disease outcome. The association between stress and decreased tolerance to disease challenge has been reviewed (Sheridan et al., 1994). One of the early physiological responses to disease and inflammation is the proinflammatory response (Baumann and Gauldie, 1994). The proinflammatory response involves a complex set of reactions involving the release of multiple soluble mediators, which impact the host’s metabolic response to inflammation (Baumann and Gauldie, 1994). An important group of soluble products of the proinflammatory response include the acute-phase proteins. In response to stress stimuli, blood concentrations of acute-phase proteins increase in cattle (Conner et al., 1988). Assessment of acute-phase protein concentrations might be a useful indicator of stress responses in calves. Therefore, the objective of this study was to determine the effect of transportation and commingling on the acute-phase protein response and performance of newly weaned beef calves.

	Materials and Methods

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Animal Care, Handling, and Diet
This study was conducted at the University of Florida Range Cattle Research and Education Center (RCREC), Ona, and at the University of Florida Beef Cattle Research Center, Gainesville. The animals utilized in this experiment were cared for by acceptable practices (FASS, 1999) approved by the University of Florida Institutional Animal Care and Use Committee (project No. A493).

Two experiments were conducted in consecutive years using newly weaned Brahman x Angus calves. In both years, study calves were weaned during the first week of August. Calves were provided with routine health management, which included deworming and vaccination for clostridial and respiratory diseases, Pasturella, Leptospirosis, and Vibriosis. To ensure that the physiological stress responses were not confounded by response to vaccination, all vaccines were administered approximately 28 d before weaning. Calves obtained for commingling treatments were obtained from a local livestock market. Although they were similar in BW, previous healthcare was unknown.

In Exp. 1, 32 newly weaned steer calves (average BW = 266 ± 20.8 kg) were randomly allotted to one of four treatments in a 2 x 2 factorial arrangement of treatments in a repeated-measures experiment. The four treatments were as follows: 1) transported and commingled, 2) not transported and commingled, 3) transported and not commingled, and 4) not transported and not commingled. Calves assigned to the transported treatment were loaded onto an open-sided livestock trailer (7.3 x 1.8 m) and transported for 3 h (344 km) to the University of Florida Beef Cattle Research Center in Gainesville. Calves assigned to the nontransported treatment remained at the RCREC where all calves were originally derived. Calves were maintained in dry lot pens of similar size (approximately 114 m²) at each location (n = four pens/treatment and eight calves/treatment). Within each transportation treatment, calves were randomly assigned to commingling treatments. Commingling was achieved by penning study calves with outsourced steer calves (n = two/pen) of a similar age and BW. Therefore, pens with treatments involving commingling had four calves/pen compared to two calves/pen for treatments without commingling. Over a 7-d sample collection period, calves were provided 3.63 kg of a medicated (100 g of chlortetracycline/ton) commercial concentrate supplement (12.0 and 72.0% CP and TDN, respectively; DM basis) and were provided ad libitum access to longstem stargrass hay (8.0 and 50.2% CP and TDN, respectively; DM basis).

In Exp. 2, 36 newly weaned calves (20 steers and 16 heifers; average BW = 222 ± 34.6 kg) were stratified by sex and randomly allotted to one of four treatments in a 2 x 2 factorial arrangement of treatments in a repeated-measures experiment. The four treatments were as follows: 1) transported and commingled, 2) not transported and commingled, 3) transported and not commingled, and 4) not transported and not commingled. Calves were derived from the RCREC. Within 3 h of weaning, calves assigned to the transported treatment were loaded onto an open-sided livestock trailer (7.3 x 1.8 m) and transported 3 h (344 km) to the University of Florida Beef Cattle Research Center in Gainesville. Calves assigned to the nontransported treatment remained at the RCREC with ad libitum access to longstem stargrass hay and water.

Upon arrival to Gainesville, transported calves were unloaded, provided access to longstem stargrass hay and water and kept overnight. In the morning, transported calves were again loaded onto the livestock trailer and returned to the RCREC. Therefore, calves in Exp. 2 were transported a total of 6 h. Upon return to the RCREC (24 h since the time of weaning) calves were put into drylot pens of equal size (114 m²; three pens/treatment and nine calves/treatment). Within each transportation treatment, calves were randomly assigned to commingling treatments. Commingling was achieved by penning study calves with outsourced steer calves (n = 2) of a similar age and BW. Therefore, pens with treatments involving commingling had five calves/pen compared to three calves/pen for treatments without commingling. Over a 21-d sample collection period calves were offered ad libitum access to a ration consisting of ground stargrass hay (11.4 and 50.9% CP and TDN, respectively; DM basis) and a medicated (100 g of chlortetracycline/ton) commercial concentrate supplement (12.0 and 72.0% CP and TDN, respectively; DM basis) at a 50:50 (concentrate:forage) ratio from d 1 to 11, and a 65:45 ratio from d 12 to 21.

Sample Collection
To investigate the influence of treatment on change in BW and acute-phase protein and cortisol concentrations, individual BW and jugular blood, obtained by venapuncture, were collected from each calf at weaning, after transport, and 1, 3, and 7 d after transport for Exp. 1, and at weaning and 1, 5, 9, 13, 17 and 21 d after transport for Exp. 2. To determine the effect of treatment on DMI, feed refusal was monitored daily for each pen in Exp. 2. All feed refused was collected, weighed, and a subsample was removed for determination of DM.

Cortisol and Acute-phase Protein Analysis
Plasma was harvested from blood following centrifugation at 2,400 x g for 20 min and then frozen at -20°C until later analysis for acute-phase protein concentration. Plasma cortisol concentrations were measured using an ¹²⁵I RIA (Coat-a-count, Diagnostic Products Corp., Los Angeles, CA) that was validated for cattle and used previously in our laboratory (Eicher et al., 2000). The cortisol intra- and interassay CV were 5.7 and 5.1%, respectively. Plasma ceruloplasmin oxidase activity was measured in duplicate using colorimetric procedures previously described (Demetriou et al., 1974). All results are expressed as mg/dL, as previously described (King, 1965). Plasma fibrinogen concentrations were determined in duplicate using a fibrinogen determination kit (Sigma procedure No. 880; Sigma Diagnostics, St. Louis, MO). Fibrinogen results were expressed as mg/dL and were determined from a standard curve generated from a human fibrinogen reference (Sigma Diagnostics). The intra- and interassay CV for ceruloplasmin and fibrinogen were controlled to values 5 and 10%, respectively. Plasma haptoglobin concentrations were determined in duplicate samples by measuring haptoglobin/hemoglobin complexing by the estimation of differences in peroxidase activity as described previously (Makimura and Suzuki, 1982). For haptoglobin concentrations 1 mg/dL, the intraassay CV are controlled to values 20%, and for concentrations >1 mg/dL, the intraassay CV are controlled to values 10%. The haptogloblin assay interassay CV is controlled to values 10%. Bovine -acid glycoprotein concentrations were measured for Exp. 2, but not Exp. 1, with a commercially available single radial immunodiffusion kit (Cardiotech; Louisville, KY). A low and high control was provided by the commercial kit, which yielded an interassay variation 4%. Serum amyloid-A concentrations were determined for Exp. 1, but not Exp. 2, with a commercially available solid-phase sandwich ELISA kit (Tridelta Ltd. Greystones, Co. Wicklow, Ireland). Intra- and interassay CV were controlled to values 10%.

Statistical Analysis
Analysis of variance for both experiments was performed using the PROC GLM procedure of SAS (SAS Inst., Inc., Cary, NC) as a split-plot in time run in a completely randomized design. In this analysis, treatment was the whole plot and day was the subplot. The model included the main effects of transportation, commingling, and day. The interactions in the model statement included transportation x commingling, day x transportation, and day x commingling. Random effects in the model were pen (transportation x commingling) and pen x day (transportation x commingling). Treatment means involving the main effects of transportation and commingling were made only when the transportation x commingling interaction was not significant. Main effects were then compared by least significant differences using the pen (transportation x commingling) mean square. Treatment means involving day were compared by least significant differences using the pen x day (transportation x commingling) mean square. With the exception of DMI measures from Exp. 2, data from outsourced calves used in commingling pens were not included in data collection or analyses.

Experiment 2 used both heifer and steer calves. Although no effects due to calf sex were expected, the original model was tested including calf sex and all possible interactions with the other model effects. Plasma cortisol concentration was the only variable that was significantly (P < 0.05) affected by sex of calf. There were no significant interactions that included sex of calf. Therefore, the model statement for the analysis of variance for plasma cortisol in Exp. 2 included the effect of calf sex and the interactions for transportation x sex, commingling x sex, and day x sex.

Percentage of change in calf BW for both experiments was analyzed using a completely randomized design with pen as the experimental unit. The model included the effect of treatment and pen, and the interaction for treatment x pen. Treatment means were compared by least significant differences using the mean square associated with the treatment x pen interaction.

	Results and Discussion

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In Exp. 1 and 2, all calves lost BW during the first day postweaning; however, transported calves lost more (P < 0.06) BW than nontransported calves from the time of weaning until the end of the transportation process (Table 1). Commingling had no effect on BW change (data not shown). In Exp. 1, transported calves lost 3.4% of their BW compared to a net average increase of 0.7% in nontransported calves from weaning to the end of the data collection period (7 d; Table 1, effect of transportation on percentage change in BW, P < 0.01). In contrast, transported calves in Exp. 2 regained lost BW faster than nontransported calves, such that the overall percentage loss of BW (weaning to d 21) tended (P = 0.09) to be less for transported (-0.4%) than nontransported calves (-2.4%; Table 1). The BW differences between Exp. 1 and 2 are likely the result of the length of data collection, whereas transported calves in Exp. 2 had 14 additional days to recover from the stress of transportation compared to calves from Exp. 1. Phillips et al. (1991b) reported a similar loss in BW for transported beef calves in one of two studies. The differences in their independent study responses were attributed to variations in climatic conditions. In their study where BW loss was observed, 80% of the weight loss was attributed to urinary losses and over 70% of the total was collected within the first 24 h. In other studies using Brahman-crossbred calves, Phillips et al. (1991a) reported greater variability in year-to-year transportation shrink than among preweaning management of calves, suggesting that annual variations associated with climatic conditions may be a major factor in BW losses of transported beef calves.

Acute-phase proteins are released from hepatocytes upon stimulation by the proinflammatory cytokines interleukin-1, interleukin-6, and tumor necrosis factor, which are central mediators of the early physiological responses to inflammation (Breazile, 1996). Analysis of circulating proinflammatory cytokines is limited in the bovine due to the lack of available antibodies essential for the development of sensitive diagnostic assays. In future studies, the incorporation of these data will provide important information for better understanding how these acute-phase proteins are responding to inflammation. Ultimately, the quantification of acute-phase protein concentrations in beef calves may provide important clues to inflammatory stress reactions to normal calf handling procedures, such as weaning, transportation, and commingling.

With the exception of haptoglobin in Exp. 1, all acute-phase proteins examined in these studies were elevated over sampling day. Results of the ANOVA are provided in Table 2 for both experiments. A nonweaned control group was not included in either study; therefore, it is not possible to determine if these increases in acute-phase protein concentrations were a direct result of weaning or maybe another inflammatory stressor. Nevertheless, similar postweaning increases in acute-phase protein concentrations were observed for both experiments, suggesting that these responses are likely attributable to the stress associated with the weaning process.

In Exp. 1, plasma cortisol concentrations were elevated (P < 0.05) at weaning compared with values obtained after transport and on d 3 and 7, but were not affected by transportation or commingling (30.6, 22.9, 25.1, 18.1, and 22.1 µg/mL for samples collected at weaning, after transport, and on d 1, 3, and 7, respectively; SEM = 2.25). Other investigators have reported an increase in plasma cortisol concentrations due to weaning (Crookshank et al., 1979). However, in contrast to the current study, their results showed a further increase in plasma cortisol concentrations as a result of transportation.

In the current study, cortisol concentration was the only variable that was affected by sex of calf. In Exp. 2, heifers had higher (P < 0.01) mean cortisol concentrations compared to steers regardless of treatment (37.0 ± 13.5 and 28.8 ± 10.6 µg/mL for heifers and steers, respectively). These data are in agreement with those of Henricks et al. (1984), who reported that heifer beef calves had higher mean plasma cortisol concentrations compared to bull calves of similar age, breeding, and management.

Each of the acute-phase proteins was increased following weaning in Exp. 2 (Table 4). With the exception of haptoglobin, neither transportation nor commingling had an effect on the proteins measured in Exp. 2 (Table 2). Average haptoglobin concentrations were higher (P = 0.04) in nontransported than in transported calves (8.42 vs. 6.06 mg/dL; SEM = 0.99). Similarly, nontransported calves had higher plasma haptoglobin concentrations compared to transported calves on d 1 and 3 in Exp. 1, respectively (Table 3). The reason haptoglobin behaved in a manner dissimilar to other acute-phase proteins in this model is unclear. The fact that this response was evident during both experiments suggests that it should not be overlooked. Unlike the other acute-phase proteins measured in this study, haptoglobin concentrations are often undetectable in unstressed cattle (Makimura and Suzuki, 1982). This characteristic should be considered when comparing its response to fibrinogen, ceruloplasmin, and -acid glycoprotein, all of which exist at basal levels in unstressed cattle.

	Implications

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	Footnotes

 
¹ Contribution No. R-09022 from the Florida Agriculture Experiment Station. Appreciation is expressed to Ms. C. Piacitelli, Ms. T. Wood, and Mr. L. Davis for their technical assistance during the conduct of these experiments.

Received for publication September 17, 2002. Accepted for publication January 13, 2003.

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