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Immune and metabolic responses of beef heifers supplemented with Saccharomyces cerevisiae to a combined viral-bacterial respiratory disease challenge

Immune and metabolic responses of beef heifers supplemented with Saccharomyces cerevisiae to a... Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers supplemented with Saccharomyces cerevisiae to a combined viral-bacterial respiratory disease challenge † † †, ‡ Alyssa B. Word,*, P. Rand Broadway, Nicole C. Burdick Sanchez, Shelby L. Roberts, ‡ || $ $ John T. Richeson, Yu L. Liang,* Ben P. Holland, Matt D. Cravey, Jimmie R. Corley, †,1 Michael A. Ballou,* and Jeffery A. Carroll *Department of Animal and Food Sciences, Texas Tech University, Lubbock, TX 79409; Livestock Issues Research Unit, USDA-ARS, Lubbock, TX 79403; Department of Agricultural Sciences, West Texas A&M || $ University, Canyon, TX 79016; Cactus Feeders, Amarillo, TX 79106; and Phileo Lesaffre Animal Care, Milwaukee, WI 53214 ABSTRACT: Two treatments were evaluated in heif- at 0, 1, 2, 3, 4, 5, 6, 7, 8, 12, 24, 36, 48, 60, and 72 h ers to determine the effects of a yeast supplement (serum isolation) relative to M.  haemolytica chal- on immune and metabolic responses to a combined lenge (0 h). Data were analyzed using the MIXED (tandem viral-bacterial) respiratory disease chal- procedure of SAS specific for repeated measures with lenge. Thirty-two beef heifers (325  ±  20.1  kg BW) fixed effects of treatment, time, and the treatment × were selected from a larger population previously time interaction. Vaginal temperature and cortisol assigned to one of two treatments: Control (CON), concentrations were similar between treatments (P receiving no yeast supplement in the diet, or yeast ≥ 0.39). Although total leukocyte count following (YST), CON diet plus a combination live yeast BHV-1 challenge was similar between treatments −1 −1 (2.5 g·heifer ·d ) and yeast cell wall (2.5 g·heif- (P = 0.21), there was a tendency (P = 0.07) for CON −1 −1 er ·d ) supplement (Phileo Lesaffre Animal Care, heifers to have greater neutrophil counts than YST Milwaukee, WI). Heifers were maintained on treat- heifers. Serum haptoglobin concentration was sim- ments for 31 d prior to the challenge. On day −3 all ilar between treatments (P = 0.13). Heifers in the heifers were fitted with an indwelling vaginal temper - YST treatment had similar serum glucose concen- ature recording device, received an intranasal chal- trations (P = 0.25) and decreased serum concentra- lenge with 2  ×  10 plaque-forming units of bovine tions of urea nitrogen compared to CON (P = 0.03). herpesvirus-1 (BHV-1), and placed in outdoor pens. Dietary treatment did not affect serum nonesterified On day 0, all heifers were fitted with an indwelling fatty acid concentrations (P  =  0.37). Nasal lesion jugular catheter, challenged intratracheally with an score severity (0–4) tended (P = 0.07) to be decreased average dose of 3.0 × 10 colony-forming units (cfu) in YST compared to CON (2.5 vs. 3.19  ±  0.26), of Mannheimia haemolytica in 100 mL media, and while water intake tended to be increased in YST were transferred into individual stanchions in an (P  =  0.06). Feeding a yeast supplement had little enclosed, environmentally controlled barn. Whole effect on the acute-phase response but improved blood samples were collected at −72 h and at 0, 2, metabolic outcomes in heifers during a respiratory 4, 6, 8, 12, 24, 36, 48, 60, and 72 h (hematology) and disease challenge. Key words: feedlot health, immune response, metabolic response, respiratory disease challenge, yeast Published by Oxford University Press on behalf of the American Society of Animal Science 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 (http://www.nationalarchives.gov.uk/doc/open-government-licence/version/2/). Transl. Anim. Sci. 2018.XX:XX–XX doi: 10.1093/tas/txy117 Corresponding author: Jeff.Carroll@ars.usda.gov Received August 20, 2018. Accepted November 5, 2018. 1 Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 2 Word et al. INTRODUCTION Committee of the Livestock Issues Research Unit (LIRU IACUC #1605F). Bovine respiratory disease (BRD) is the lead- Yeast additive was a combination yeast cell ing cause of morbidity and mortality in U.S. feed- wall and live yeast product developed from a lots (USDA, 2013a), with 16% of cattle requiring primary S.  cerevisiae yeast strain. Thirty-two BRD treatment during the feeding period (USDA, British crossbred heifers were obtained from a 2013b). Losses in live performance or carcass value commercial feedlot in the Texas panhandle and may be experience by cattle diagnosed with BRD transported approximately 112 km to the USDA- even after clinical signs subside (Duff and Galyean, ARS Livestock Issues Research Unit’s Research 2007). While BRD is a multifaceted disease, sev- Complex in New Deal, TX. Two treatments were eral known viral and bacterial pathogens have been evaluated: 1)  Control (CON) receiving no yeast reported to be causal factors, including bovine additive in the diet, or 2) CON diet plus 2.5 g·heif- herpesvirus-1 (BHV-1) and Mannheimia haemolyt- −1 −1 −1 −1 er ·d live yeast and 2.5 g·heifer ·d yeast cell ica (Duff and Galyean, 2007). Currently, 59% of −1 −1 wall, dosed to 8 g·heifer ·d with carrier (YST, feedlots treat at least some cattle with metaphylaxis Phileo Lesaffre Animal Care, Milwaukee, WI). The to control BRD (USDA APHIS, 2013b), a process live yeast was fed to 25 × 10 colony-forming units that is under scrutiny for the judicious use of anti- −1 −1 (cfu)·heifer ·d . Heifers were chosen from a larger microbials (Dennis et  al., 2018). Methods to pre- herd of 560 heifers per treatment which had been vent or control BRD are therefore needed. received at a commercial feeding facility 35 d prior Yeast supplementation, specifically to transport to the USDA facilities. Processing at Saccharomyces cerevisiae supplementation, may the commercial feeding facility included individ- serve as a means of altering beef cattle response to ual identification with uniquely numbered ear tags, BRD during the feeding period (Finck et al., 2014). treatment with an endectocide (Cydectin Injectable, Yeast cell wall contains β-glucans that have been Bayer Animal Health, Whippany, NJ), vaccina- reported to activate macrophage and neutrophil tion against viral diseases (Vista 5 SQ, Merck function in mice (Akramiene et  al., 2007). These Animal Health, Summit, NJ) and clostridial dis- β-glucans are associated with improved immune eases (Ultrabac 7, Zoetis, Florham Park, NJ), and function (Broadway et al., 2015) and therefore health administered an anabolic implant (Revalor-IH, of newly received feedlot cattle (Keyser et al., 2007). Merck Animal Health). Heifers were selected for Live yeast and yeast cell wall supplements may each the current trial from the larger herd in order to bind pathogenic microorganisms such as Salmonella select a sample with similar phenotype. Selection or Escherichia coli and prevent colonization of these criteria included black hided cattle without visi- bacteria in the gastrointestinal tract (Perez-Sotelo ble Brahman influence, cattle with a similar tem- et  al., 2005; Posadas et al., 2017). While the mech- perament using the pen and chute scoring system anism of action is not completely understood, yeast described by King et al. (2006), uniformity of BW, supplements have altered morbidity and mortality in and average serum antibody titer against BHV-1 feedlot cattle (Keyser et al., 2007; Finck et al., 2014), of 16 for each treatment (Texas A&M Veterinary and may reduce immune response severity and neg- Diagnostic Laboratory, Amarillo, TX). Blood for ative metabolic outcomes (Burdick Sanchez et  al., serum was collected on a larger sample of cattle at 2013, 2014). Therefore, the objective of the current the commercial facility and analyzed for serum anti- study was to evaluate the effects of a supplement body titer against BHV-1 prior to arrival at USDA containing live S. cerevisiae and S. cerevisiae cell wall facilities. The scoring system outlined by King et al. components on the immune and metabolic outcomes (2006) was used to assign cattle to subjective pen of feedlot heifers administered a combined viral and scores prior to being processed where 1  =  walks bacterial BRD challenge. The experimental hypothe- slowly, can be approached slowly, not excited by sis was that supplementing heifers with yeast for 31 d humans; 2 = runs along fences, stands in corner if prior to the BRD challenge would improve immune humans stay away; 3 = runs along fences, head up and metabolic responses to a BRD challenge. and will run if humans approach but stops before hitting gates and fences; 4 = runs, stays in back of MATERIALS AND METHODS group, head high and aware of humans, may run into fences and gates; 5 = excited, runs into fences All experimental procedures were in com- or anything in path. Chute scores were assigned as pliance with the Guide for the Care and Use of cattle were processed where 1 = calm, no movement; Agricultural Animals in Research and Teaching and 2  =  slightly restless; 3  =  squirming, occasionally approved by the Institutional Animal Care and Use Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 3 shaking the chute; 4  =  continuous, very rigorous finish diet for RAMP at 15% intervals every 2 to 4 movement and shaking of the chute; 5  =  rearing, d. Feed was transported every 3 d from commercial twisting of the body and struggling violently. Pen facilities to USDA facilities after cattle were trans- and chute score were then averaged to assign each ported, and stored in a tarp-covered trailer inside a heifer a temperament score, and animals were cho- covered, temperature-controlled barn. Average ini- sen based on an average score of less than 3.  All tial BW of the cattle transported to USDA facilities heifers selected had not received treatment for was 325 ± 20.1 kg. Following arrival at the USDA clinical BRD during the feeding period. All heif- facility, heifers were allowed to rest overnight in dirt ers had been randomized to treatment group and pens (7.6  ×  18.3 m) and were maintained on the maintained on respective treatments (n  =  16 per respective treatment diets previously assigned at the treatment) for 31 d prior to arrival at the USDA commercial feeding location, with ad libitum access facilities for a commercial research trial evaluating to water. On study day −3, heifers were weighed the same yeast product used in the current study. and fitted with a vaginal temperature recording At the commercial facility, heifers were fed 100% device. Briefly, a temperature sensor (Star-ODDi RAMP (Cargill Corn Milling, Bovina, TX) and DST micro-T; MeterMall USA, Marysville, OH) transitioned to the same diet fed at the USDA facil- was secured into a blank controlled internal drug ities (Table  1) by incremental substitution of the release (CIDR) device (Pfizer Animal Health, Sterling, CO) as described by Burdick et al. (2011), Table 1. Ingredient formulation and analyzed com- which was then placed using a CIDR applicator position of finish diets into the vagina of each heifer. Vaginal tempera- ture was measured every 5 min from insertion until Finish diet formula- the completion of the study. A  nasal lesion score tions (% of DM) was also recorded at this time where 0  =  absence Ingredient of lesions; 1  =  less than 10% coverage of the vis- Corn, steam flaked 58.5 Corn distillers grain, wet 17.1 ible naris; 2  =  11% to 25% coverage; 3  =  26% to Wet corn gluten feed 16.1 50% coverage; and 4 = 50% or greater coverage of Corn stalks, chopped 7.2 the visible naris. All heifers were challenged intra- Fat 1.1 nasally at this time with approximately 2  ×  10 Additives plaque-forming units (pfu) of BHV-1. For the Vitamin A, IU/kg 2,645 BHV-1 dose, a single vial of BHV-1 was diluted to Vitamin D, IU/kg 264.6 a final concentration of 1 × 10 pfu/mL, and then −1 −1 Melengesterol acetate, mg·heifer ·d 0.40 1  mL of diluted virus was administered per naris Monensin, mg/kg 46.85 in each heifer using a syringe and a nasal atomiza- Tylosin, mg/kg 10.69 tion device. Whole blood was collected into a 4-mL 4 5 Analyzed composition (% of DM) CON YST tube containing 7.2  mg K EDTA (Vacutainer; Dry matter 60.3 60.8 Becton, Dickinson, and Company, Franklin Lakes, Crude protein 15.1 15.3 NJ) and blood for serum isolation collected into Equivalent crude protein 1.0 1.0 a 9-mL tube (Vacutainer; Becton, Dickinson, and Neutral detergent fiber 20.8 20.9 Company, Franklin Lakes, NJ) containing no addi- Fat 5.2 5.2 tive via jugular venipuncture prior to challenge. Ca 0.74 0.70 All heifers were then returned to the outdoor pens P 0.51 0.51 and were monitored daily for clinical symptoms of Mg 0.24 0.24 BRD. Indwelling vaginal temperature recording K 0.81 0.82 devices were removed on study day 3. S 0.25 0.25 The morning of study day 0, heifers were fitted Sweet Bran wet corn gluten feed (Cargill Corn Milling, Bovina, TX) with an indwelling jugular catheter. Whole blood with added calcium carbonate (4% as fed), salt (1.8%), urea (1.1%), and blood for serum was collected via the jugu- and trace mineral premix (0.2%). lar catheter and heifers were challenged with log- Rumensin 90, Elanco Animal Health. Tylosin 100, Elanco Animal Health. arithmic phase culture M.  haemolytica in 100  mL Reported by Servi-Tech Laboratories, Amarillo, TX. Values are media. Four batches of M. haemolytica were made means (n = 7). and heifers received the challenge in blocks of eight Treatments were: 1) negative control (CON) fed a standard finish- heifers to ensure that each received log phase cul- −1 −1 ing diet, or 2)  YST, fed the same finishing diet with 2.5 g·heifer ·d −1 −1 ture. Mannheimia haemolytica titers (cfu counts) live yeast and 2.5 g·heifer ·d yeast cell wall (Phileo Lesaffre Animal Care, Milwaukee, WI). were determined by serial dilution and plating Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 4 Word et al. immediately prior to the first animal receiving the using a commercially available enzyme immuno- intratracheal challenge and immediately following assay kit according to the manufacturer’s directions the eighth (final) animal challenged for each batch. (Arbor Assays, Ann Arbor, MI) by compari- Each batch was measured on a UV visible spectro- son of unknowns to standard curves generated photometer at 590 nm to a transmittance between with known concentrations of cortisol. Minimum 62% and 68%. Based on this, the average dose of detectable cortisol concentration was 0.4  ng/mL, the four batches was 3.0 × 10 cfu of M. haemolyt- and the intra- and inter-assay coefficients of var - ica. Each heifer was challenged with the prepared iation were 10.6% and 4.2%, respectively. Serum M.  haemolytica via intratracheal injection using a haptoglobin concentrations were also determined 16 gauge, 25.4 mm needle and two 60 mL syringes. using a commercially available enzyme immuno- Heifers were then moved to individual stalls (2.28 assay kit according to the manufacturer’s direc- m in length, 0.76 m in width, and 1.67 m in height). tions (Immunology Consultants Laboratory, Inc., Heifers were fed a complete finishing diet (Table 1) Portland, OR). Intra- and inter-assay coefficients once daily ad libitum such that each heifer was of variation were 6.0% and 15.3%, respectively. offered 4.5 kg of fresh feed each morning and orts Glucose concentrations were determined by were discarded (Table  1). Yeast supplement was modification of the enzymatic Autokit glucose hand mixed into the daily ration while heifers were (Wako Pure Chemical Industries, Chuo-Ku, Osaka, in the stanchions to the appropriate treatments. Japan) to fit a 96-well format, where 300  µL of pre- Prior to the immunological challenge, no feed was pared working solution was added to 2 µL of serum discarded, although yeast treatment may have been or prepared standards in a 96-well plate. Plates were included in feed that was refused by heifers dur- incubated at 3 °C for 5 min and then read using a ing the immunological challenge and subsequently plate reader at 505  nm. Concentration of glucose discarded. Individual water intake was measured was determined by comparing unknown samples to from 0 to 72 h while heifers were housed in individ- a standard curve of known glucose concentrations. ual stanchions via a Suevia Cup (QC Supply Inc., Minimum detectable concentration was 3.8 mg/dL Schuyler, NE). Whole blood was collected in 4-mL and intra- and inter-assay coefficients of variation tube containing 7.2  mg K EDTA at 0, 2, 4, 6, 8, were 7.4% and 10.7%, respectively. 12, 24, 36, 48, 60, and 72  h post-M.  haemolytica Serum nonesterified fatty acid (NEFA) concen- challenge via the jugular catheter. Blood for serum trations were determined by modification of the was collected in 9-mL Sarstedt tubes containing no enzymatic HR Series NEFA-HR (2) assay (Wako additive (Sarstedt, Inc., Newton, NC) every hour Diagnostics, Richmond, VA) to fit a 96-well format until hour 8, at 12 h, and then every 12 h until 72 h where 200 µL of the Color Reagent A were added via the jugular catheter. Blood for serum was incu- to 5 µL of serum or prepared standards in a 96-well bated at room temperature for 30 min and then cen- plate. Plates were incubated at 37 °C for 5 min and trifuged at 1,500 × g for 20 min at 4 °C and serum then the absorbance was read using a spectropho- removed and frozen at −80 °C. Following the col- tometer at 550 nm. Next, 100 µL of Color Reagent lection of the 72  h sample, heifers were weighed, B was added to all wells on the 96-well plate. Plates jugular catheters were removed, and all heifers were incubated for an additional 5  min and read were treated with florfenicol (Nuflor Gold, Merck for a second time using a plate reader at 550  nm. Animal Health, Madison, NJ) by subcutaneous A  final absorbance was obtained by subtracting injection at 40  mg florfenicol/kg body weight to the first reading, which was multiplied by a factor treat the known bacterial (M.  haemolytica) infec- of 0.67 to account for changes in volume, from the tion that had been administered to the animals. second reading. The final absorbance values were Whole blood samples were analyzed for hema- used for all calculations. Concentrations of NEFA tology, including: total leukocyte counts, leukocyte were determined by comparing unknown samples differential, hematocrit, and hemoglobin using to a standard curve of known NEFA concentra- an IDEXX Procyte Dx Hematology Analyzer tions. The minimum detectable concentration (IDEXX Labs, Westbrook, ME) with bovine-spe- was 0.021  mmol/L and the intra- and inter-assay cific algorithms. Whole blood was also collected coefficients of variation were 8.8% and 10.5%, in heparinized tubes at −72, 0, and 48 h relative to respectively. M.  haemolytica challenge and analyzed to deter- Concentrations of serum urea nitrogen were mine polymorphonuclear (PMN) leukocyte activity. determined by a colorimetric assay according to the All serum analyses were performed in duplicate. manufacturer’s directions (K024-H1; Arbor Assays, Serum cortisol concentrations were determined Ann Arbor, MI) by comparison of unknowns to Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 5 standard curves generated with known concentra- sample collected at 0 h was analyzed due to differ- tions of urea nitrogen. The minimum detectable ences between treatment at 0 h. Nasal lesion scores concentration was 0.093  mg/dL and intra- and were analyzed using the GLIMMIX procedure of inter-assay coefficients of variation were 12.8% and SAS with fixed effects of treatment, time, and the 8.7%, respectively. treatment × time interaction. All data presented are Neutrophil functionality was determined by as LSM ± SEM with P ≤ 0.05 considered significant the phagocytic and oxidative burst capacity against and 0.05 < P ≤ 0.10 considered a tendency. an environmental E.  coli as well as the surface expression of the adhesion molecule, CD62L (i.e., RESULTS L-selectin), as described by Obeidat et  al. (2013). No treatment × time interaction occurred Briefly, oxidative burst intensity and phagocytic (P  =  0.84) for vaginal temperature, and tempera- activity was determined by incubating 200  µL of ture was similar (P = 0.39) between CON and YST whole blood in an ice bath and then combining (Figure  1; 39.4  ±  0.08 vs. 39.3  ±  0.08  °C, respec- with 40 µL each of 100 µM dihydrorhodamine and tively). Vaginal temperature increased (P  <  0.001) heat-killed E. coli at 1 × 10 cells per mL. Samples for 10  h in both treatments following the BHV- were incubated in a 38.5 °C water bath for 10 min, 1/M. haemolytica challenge with a peak of 40.2 °C then subsequently placed in an ice bath for 15 min occurring at 10  h. Water intake, and hematologi- to stop the reaction, hypotonically lysed, and then cal measures are reported in Table 2. There was no washed with ice cold phosphate-buffered saline treatment × time interaction (P  =  0.52) for water (PBS). A  BD Accuri flow cytometer was used to intake, and total water intake tended to be greater analyze leukocytes, and neutrophils were gated on (P = 0.06) in the YST treatment compared to CON the scatterplot of forward scatter × side scatter. (676  ±  32.3 vs. 588  ±  32.3  mL/h, respectively). Data are reported as the percentage of neutrophils Water intake fluctuated over time following viral that were positive for phagocytosis and oxida- challenge (P < 0.01). tive burst as well as the mean fluorescence inten- No treatment × time interaction occurred sity of the positive populations. Negative controls (P  =  0.98) for serum cortisol concentration included E.  coli only, remained on ice throughout (Figure  2). Serum cortisol was similar (P  =  0.90) the dihydrorhodamine, and incubated with remain- between treatments (20.7 ± 1.14 vs. 20.5 ± 1.14 ng/ ing samples. The surface expression of L-selectin mL for CON and YST, respectively). Serum cortisol was determined by incubating 50  µL of whole concentration was greatest at time of M. haemolyt- blood with anti-bovine CDL62L (monoclonal ica challenge and decreased over time (P < 0.01). No antibody IgG1-isotype in the mouse; VMRD Inc., treatment × time interaction (P = 0.23) occurred for Pullman, WA) at a final dilution of 5  µg/mL for 1 h any hematological measure. Hematological meas- in an ice bath, then hypotonically lysed and rinsed ures, except for neutrophil concentrations, were with PBS. The pellet was resuspended in fluoresce- not different (P ≥ 0.16) between treatments. Total in-labeled secondary antibody and incubated on ice neutrophil concentration tended (P  =  0.07) to be for 1 h, then washed twice using PBS and analyzed greater in CON heifers (6.4 ± 0.39 vs. 5.4 ± 0.37 10 using flow cytometry as described above. The nega- cells per µL, respectively). Number of neutrophils in tive control was secondary antibody only. Data are circulation increased following live pathogen chal- reported as the mean fluorescence intensity of each lenge until hour 8 and then decreased (P  <  0.01). sample. No treatment × time interaction occurred (P ≥ Vaginal temperature data were averaged into 0.47) for any measure of neutrophil functionality. 1-h intervals for analysis. Hematological, meta- Neutrophil phagocytosis, oxidative burst inten- bolic, and temperature data were analyzed using sity, and expression of L-selectin were not differ- the MIXED procedure of SAS specific for repeated ent between treatments (P ≥ 0.13). Oxidative burst measures (SAS Institute Inc., Cary, NC) with fixed intensity and expression of L-selectin increased in effects of treatment, time, and the treatment × both treatments over time (P  <  0.001). There was time interaction. The autoregressive (1) covariance no treatment × time interaction (P  =  0.94) for structure for the within-subject measurement was serum haptoglobin concentration. Haptoglobin used in all models except for vaginal temperature was not different (P  =  0.13) between treatments data, where the compound symmetry covariance (15,396.2  ±  1,631.7 vs. 11,757.3  ±  1,631.7  µg/ structure was used. Covariance structures were dL; P  =  0.13; Figure  3), although haptoglobin chosen based on the smaller Bayesian Information increased (time effect: P < 0.01) in both treatments Criterion. For serum glucose, change relative to the Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 6 Word et al. CON YST Ambient 40.4 39.6 40.2 39.4 39.2 39.8 39.6 38.8 39.4 39.2 38.6 38.4 38.8 38.2 38.6 38.4 38.2 37.8 -4 -1 2 5 8 11 14 17 20 23 26 29 32 35 38 41 44 47 50 53 56 59 62 65 68 71 Hour relative to M. haemolytica challenge Figure  1. Effect of yeast supplementation on vaginal temperature response in beef heifers (n  =  16/trt). Heifers were fed one of two dietary −1 −1 treatments: 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 −1 −1 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged 8 7 intranasally with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means. There was no treatment × time interaction (P = 0.84) and vaginal temperature was not affected by dietary treatment (P = 0.39), although temperature decreased over time (P < 0.01). Treatment means were 39.4 ± 0.08 for CON and 39.3 ± 0.08 °C for YST. SEM = 0.084. Table  2. Effect of yeast supplementation on vaginal temperature, water intake, nasal lesion score, serum and hematology variables, and neutrophil functionality in feedlot heifers administered a respiratory disease challenge Treatment Item CON YST SEM P-value Vaginal temperature, °C 39.4 39.3 0.08 0.39 Water intake, mL/h 588 676 32.3 0.06 Serum haptoglobin, µg/dL 15,396 11,757 1,631.7 0.13 Serum cortisol, ng/mL 20.7 20.5 1.14 0.90 Lymphocytes, 10 /µL 4.65 4.59 0.26 0.86 Neutrophils, 10 /µL 6.39 5.37 0.39 0.07 Neutrophil:Lymphocyte 1.50 1.35 0.12 0.36 Platelets, 10 /µL 438.8 399.3 30.5 0.36 Red blood cells, 10 /µL 7.60 7.29 0.15 0.17 Eosonophils, 10 /µL 0.18 0.17 0.03 0.72 Hematocrit, % 34.3 33.8 0.48 0.43 Hemoglobin, g/dL 11.2 11.0 0.13 0.16 Monocytes, 10 /µL 1.60 1.64 0.073 0.65 Neutrophil oxidative burst intensity, GMFI 119,898 135,696 7,227.5 0.13 PMN phagocytosis, GMFI 47,013 45,867 2,650.8 0.76 L-Selectin expression, GMFI 98,030 103,914 3,966.3 0.30 Heifers were fed one of two dietary treatments: 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with −1 −1 −1 −1 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) 31 d prior to immunological challenge (YST). Whole blood was collected every 2 h from 0 to 8 h and every 12 h from 12 to 72 h for hematology, and every 1 h from 0 to 2 h and every 12 h from 12 to 72 h for serum analysis. Represents treatment P-value. All treatment × time interactions were P ≥ 0.19. Geometric mean florescence intensity (GMFI) for neutrophil oxidative burst intensity, phagocytosis, and L-selectin expression. Whole blood was collected −72, 0, and 48 h relative to Mannheimia haemolytica immunological challenge. and remained so through the final sampling time There was a trend (P = 0.04) for a treatment × point at 72 h following the BHV-1/M. haemolytica time interaction for serum glucose where CON challenge. heifers had decreased serum glucose at 1  h and Translate basic science to industry innovation Vaginal temperature (°C) Ambient temperature (°C) Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 7 CON YST 01234567 8122436486072 Hour relative to M. haemolytica challenge Figure 2. Effect of yeast supplementation on serum cortisol response in beef heifers (n = 16/trt). Heifers were fed one of two dietary treatments: −1 −1 −1 −1 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged intranasally 8 7 with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means ± SEM. There was no treatment × time interaction (P = 0.98) and serum cortisol was not affected by dietary treatment (P = 0.90), although serum cortisol decreased over time (P < 0.01) as cattle adapted to stanchions. CON YST -10000 0 1234567 8122436486072 Hour relative to M. haemolytica challenge Figure  3. Effect of yeast supplementation on serum haptoglobin response in beef heifers (n  =  16/trt). Heifers were fed one of two dietary −1 −1 treatments: 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 −1 −1 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged 8 7 intranasally with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means ± SEM. There was no treatment × time interaction (P = 0.94) and serum haptoglobin was not affected by dietary treatment (P = 0.13), although serum haptoglobin increased over time (P < 0.01). remained so until 6 h following BHV-1/M. haemo- YST, respectively; Figure  5). Serum urea N was lytica challenge, at which time the treatments were greater (P = 0.03) in the CON treatment compared similar. Serum glucose concentration was similar to YST (11.8 ± 0.53 vs. 10.1 ± 0.53 mg/dL, respec- between treatments (P  =  0.25; Figure  4). There tively; Figure 6). Serum urea N generally increased was no treatment × time interaction (P ≥ 0.65) for over time following BHV-1/M.  haemolytica chal- serum NEFA or urea N concentrations. Serum lenge (P  <  0.001). Nasal lesion scores recorded 6 NEFA increased in both treatments from 0 to 12 h, d following BHV-1 challenge tended (P = 0.07) to and subsequently decreased (time P < 0.01), but be more severe in CON heifers compared to YST was not different (P  =  0.37) between treatments (Figure 7). However, heifers in both treatments pre- (0.15 ± 0.01 vs. 0.14 ± 0.01 mmol/L for CON and sented with nasal lesions of varying severity. Translate basic science to industry innovation Serum haptoglobin (µg/dL ) Cortisol concentration, ng/mL Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 8 Word et al. -20 CON -40 YST -60 -80 -100 -120 -140 12345678 12 24 36 48 60 72 Hour relative to M. haemolytica challenge Figure 4. Effect of yeast supplementation on serum glucose response in beef heifers (n = 16/trt). Heifers were fed one of two dietary treatments: −1 −1 −1 −1 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). Data presented as least squares means ± SEM and 0 h was used as a covariate in the analysis. All heifers were challenged intranasally with 2 × 10 plaque-forming units bovine herpesvirus-1 (BHV-1) at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. There was a tendency for a treatment × time interaction (P = 0.04) such that CON heifers had decreased serum glucose at 1 h and remained so until 6 h following BHV-1/M. haemolytica. Serum glucose was similar between dietary treatments (P = 0.25). 0.3 0.25 0.2 0.15 CON YST 0.1 0.05 01234567 8122436486072 Hour relative to Mannheimia haemolytica challenge Figure 5. Effect of yeast supplementation on serum NEFA response in beef heifers (n = 16/trt). Heifers were fed one of two dietary treatments: −1 −1 −1 −1 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged intranasally 8 7 with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means ± SEM. Serum NEFA was not affected by dietary treatment (P = 0.37) and there was no treatment × time interaction (P = 0.88). DISCUSSION at 0  h. Peak temperatures (40.2  °C in both treat- ments) were similar to the threshold (40 °C) febrile Dietary treatment did not affect vaginal tem- response reported by Perino and Apley (1998) for perature in the current study. In contrast, Finck BRD treatment in feedlots. Average temperature et al. (2014) reported decreased rectal temperature in each treatment group in this trial was near the following an lipopolysaccharide (LPS) challenge threshold for clinical illness outlined by Duff and in steers fed yeast cell wall or a combination live Galyean (2007), and is similar to a febrile response and yeast cell wall compared to a negative con- from which cellular immunological responses could trol. Vaginal temperature increased in all treat- ments when calves were experimentally challenged be anticipated (Thomson et al., 1975). Although Translate basic science to industry innovation Serum non-esterfied fatty acid (mmol/L) Change in glucose concentration (mg/dL) Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 9 CON YST 0 12345678 12 24 36 48 60 72 Hour relative to Mannheimia haemolytica challenge Figure  6. Effect of yeast supplementation on serum urea nitrogen response in beef heifers (n  =  16/trt). Heifers were fed one of two dietary −1 −1 treatments: 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 −1 −1 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged 8 7 intranasally with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means ± SEM. Serum urea nitrogen was decreased in YEAST compared to CON (P = 0.03) and there was no treatment × time interaction (P = 0.65). the current study collected vaginal temperature, meeting outlined requirements for water intake rectal and vaginal temperatures have been reported in finishing cattle (NRC, 2000). However, hemat- to be highly correlated during immunological ocrit percentage and other hematological measure- challenges (Burdick et al., 2011; Falkenberg et al., ments were similar between treatments and were 2014). Jericho and Langford (1978) established an within the range of what is considered normal in interaction between BHV-1 and M.  haemolytica beef cattle (Radostits et  al., 2000) so water intake in BRD when they reported fibrous pneumonic is not expected to have affected the interpretation lesions similar to lesions occurring in field BRD of hematological or other measures reported in calves experimentally challenged with these path- this trial. ogens, dependent on a 3- to 5-d interval between Nasal lesion scores tended to be more severe viral and bacterial inoculation similar to the in the CON treatment. Ulcerated nasal mucosa is interval used in the current trial. Vaginal temper- a symptom of respiratory infection with BHV-1, ature also fluctuated within each day, which was and leads to the more severe “red nose” infection expected. Although heifers were housed in an envir- frequently associated with infectious bovine rhi- onmentally controlled barn, daily ambient temper- notracheitis (Nandi et  al., 2009). Heifers in both ature fluctuations occurred, which paired with the treatment groups exhibited nasal lesion scores ≥1 circadian rhythm of vaginal temperature may have and had lesions of varying severity present; there- resulted in the daily fluctuations observed. Burdick fore, the BHV-1 challenge did successfully elicit et al. (2011) reported that the vaginal temperature clinical signs of an immune response in both treat- devices used in the current trial are capable of meas- ment groups. uring the circadian rhythm in vaginal temperature. Dietary treatment did not affect serum cortisol Water intake was greater in the YST treatment concentration in the current study. This response compared to CON. Previous literature has reported is similar to the serum cortisol response observed that frequency and duration of water intake was by Burdick Sanchez et al. (2013), who reported no similar (Sowell et al., 1999) or increased (Buhman difference when beef heifers were supplemented et  al., 2000) in feedlot cattle that were clinically with yeast cell wall compared to a negative con- ill compared to healthy cattle. Water is required trol and challenged with LPS. In contrast, Finck for multiple maintenance functions including reg- et al. (2014) reported that feeding combination live ulation of body temperature, metabolism, and yeast and yeast cell wall to beef steers decreased transportation of cells through the bloodstream, serum cortisol concentrations compared to a neg- including immune cells. In terms of total daily ative control following an LPS challenge. In the intake, heifers in both treatment groups were not current study, increased cortisol production due Translate basic science to industry innovation Serum urea nitrogen (mg/dL) Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 10 Word et al. CON 3 YST 0 1234 Nasal Lesion Score Figure 7. Effect of yeast supplementation on nasal lesion scores (0–4) in beef heifers (n = 16/trt) All heifers were challenged intranasally with 8 7 2 × 10 plaque-forming units bovine herpesvirus-1 (BHV-1) at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h and scores were collected 72 h following BHV-1 challenge. Heifers were fed one of two dietary treatments: 1) negative control (CON), fed a standard feedlot −1 −1 −1 −1 diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). Score was determined according to the following criteria: 0 = absence of lesions; 1 = less than 10% coverage of the visible naris; 2 = 11% to 25% coverage; 3 = 26% to 50% coverage; and 4 = 50% or greater coverage of the visible naris. Data presented as number of animals receiving a score within each category. Nasal lesion scores tended (P = 0.07) to be more severe in CON compared to YST. to stress during processing and administration of greater probability for long-term tissue damage the bacterial challenge marked a rapid increase in as neutrophils undergo apoptosis or migrate into circulating cortisol in both treatments. However, peripheral tissue, expression of L-selectin was not serum cortisol concentrations in both treatments different between treatments in the current trial. were greatest immediately following M.  haemo- Therefore, the tendency for increased circulating lytica challenge and decreased at each subsequent neutrophils was not explained by decreased chemo- time point. Such a response suggests that heifers taxis mediated by L-selectin. Results for both may have been stressed due to handling involved treatments agree with the literature as expression with catheterization and challenge, but serum cor- of L-selectin increased over time in conjunction tisol concentrations decreased as heifers became with decreased circulating cortisol (Burton et  al., adapted to the stanchions. Therefore, there appears 1995). In contrast to Akramiene et al. (2007), PMN to be no cortisol response directly to the viral-bac- phagocytosis and oxidative burst intensity in the terial challenge. current trial were not different between treatments A tendency for greater circulating neutrophil but generally increased following M.  haemolytica concentrations occurred in CON compared to YST challenge as neutrophils became active in tissue in the current trial. While the mode of action of and began phagocytizing and ultimately destroying yeast products has not been clearly defined, cell bacterial pathogens. wall of S.  cerevisiae contains β-glucans that have Serum haptoglobin concentrations were similar also been reported to enhance phagocytic activity between CON and YST treatments following the of neutrophils in vitro (Akramiene et  al., 2007). BHV-1/M.  haemolytica challenge. Haptoglobin is Neutrophil concentration in circulation has also an acute-phase protein secreted from hepatocytes been reported to increase in the presence of glu- during inflammation, is undetectable in healthy cocorticoids, as L-selectin expression and there- calves, and could take up to 4 to 8 d after live fore chemotaxis of neutrophils into peripheral pathogen infection to be detectable in sick cattle tissues decreases in the presence of glucocorticoids (Ganheim et  al., 2003). In the current study, data (Burton et  al., 1995). However, these neutrophils were only collected for 6 d following BHV-1 inoc- may exhibit a “rebound effect” after circulating ulation, which may not have been enough time to glucocorticoids decrease that allow chemotaxis measure peak haptoglobin response. Future stud- into peripheral tissues, increasing phagocytic activ- ies should collect serum haptoglobin concentra- ity and thereby lung tissue damage in the case of tions for up to 14 d, as concentrations may begin to BRD-affected calves (Burton et  al., 2005). While return to normal after 13 d (Ganheim et al., 2003). increased circulating neutrophils may indicate Acute-phase protein production from hepatocytes Translate basic science to industry innovation Number of heifers scored in each category, n Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 11 is stimulated by pro-inflammatory cytokines, spe- Immunological insults initially induce hyperg- cifically IL-6 (Naka et al., 2002). Burdick Sanchez lycemia, as has been demonstrated during the stress et  al. (2013) reported that serum IL-6 concentra- response, and subsequently cause hypoglycemia tion was decreased in cattle supplemented with a in response to increased metabolic demands for similar yeast cell wall product when compared to a energy. Waggoner et  al. (2009) reported that beef negative control following LPS challenge. In con- steers challenged with LPS initially increased above trast, Zaworski et al. (2014) reported no difference and subsequently decreased below the serum glu- in serum haptoglobin concentration postpartum cose concentration of an unchallenged cohort, sug- in dairy cows supplemented with S.  cerevisiae. gesting an initial increase during the inflammatory However, these authors did report increased Serum response and a decrease as cattle use the energy Amyloid A  concentration 1 d after calving in to deal with the immunological challenge, which cows supplemented with S.  cerevisiae, which they could explain the rapid increase at 5  h and subse- hypothesize may be beneficial after calving because quent decrease reported in the current trial. When acute-phase protein production creates a negative testing for a metabolite that could aid in the predic- feedback loop that downregulates the production tion of BRD outcomes, Montgomery et al. (2009) of pro-inflammatory cytokines. reported a linear decrease in blood glucose concen- Immune responses to an immunological insult tration measured on-arrival as subsequent number require large amounts of energy and potentially of BRD treatments during the receiving period change nutrient partitioning. A  1  °C increase in increased. The authors hypothesized cattle with body temperature increases resting metabolic rate decreased blood glucose on-arrival that were later by 10% to 20% in mice (Buchanan et al., 2003), and treated for BRD may have been exposed to path- further energy is required to produce acute-phase ogens prior to arrival and experienced hypoglyce- proteins and other mediators of inflammation and mia on-arrival because they were already fighting the immune response (Carroll and Forsberg, 2007). disease. Serum glucose concentration in the current In the current study, there was a treatment effect trial was decreased in the CON treatment from 1 to for serum glucose concentrations where serum glu- 5 h compared to the YST treatment, in line with the cose was greater in the YST treatment compared initial decrease that Montgomery et al. (2009) and to CON. The increase in glucose concentration in Waggoner et al. (2009) have suggested to be indic- the YST group may imply that a greater amount of ative of disease risk and indicates that cattle were readily available glucose was being utilized in the already responding to the BHV-1 challenge prior to CON treatment compared to the YST, potentially the M. haemolytica challenge administered at 0 h. to meet increased metabolic requirements of the Serum NEFA concentrations were similar immune system. Cytokines were reported to stimu- between CON and YST treatments. In contrast, late hepatic gluconeogenesis while increasing over- previous studies have reported both decreased all utilization of glucose in mice and pigs (Lang IL-6 production and subsequent decreased serum and Spitzer, 1987; Webel et  al., 1997), although NEFA concentration in cattle fed yeast cell wall this proposed mechanism cannot be confirmed as compared to a negative control when each were cytokines were not measured in the current study. challenged with LPS (Burdick Sanchez et  al., When challenging with LPS and feeding a yeast cell 2013, 2014). Exposure to endotoxin induced wall, Burdick Sanchez et al. (2014) reported no dif- hypertriglyceridemia by inhibiting lipoprotein ference in serum glucose concentration compared lipase activity and inducing hepatic fatty acid syn- to a negative control, although insulin concentra- thesis in rats, which is stimulated in part by pro- tion was greatest in cattle supplemented with yeast duction of the pro-inflammatory cytokine IL-6 cell wall, which is in contrast with results of the cur- (Hardardottir et  al., 1994). The authors explain rent trial. However, Zaworski et al. (2014) reported benefits of these metabolic changes include meet- a tendency for increased serum glucose and serum ing increased metabolic needs and the ability of urea nitrogen postpartum in dairy cows fed a lipoproteins to both bind endotoxin and inhibit S.  cerevisiae strain, which the authors propose to viral replication. An increase in serum NEFA in be a faster transition out of a negative energy bal- all treatments following BHV-1/M.  haemolytica ance postpartum. Metabolic results of that study challenge in the current trial could be the mixed could be in agreement with results of the current result of cattle in both treatments needing to meet study, where increased serum glucose concentration the energetic requirements of the immune system is considered desirable because cattle are not parti- and altered need for antiviral mechanisms follow- tioning that energy elsewhere. ing the viral challenge. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 12 Word et al. Serum urea N was increased in the CON with yeast and exposed to an immunological chal- treatment compared to YST in the current study. lenge. While nasal lesion scores tended to be less Pro-inflammatory cytokines have been reported severe and neutrophil concentration tended to be to increase catabolism of lean tissue in pigs decreased when cattle were supplemented with (Hardardottir et  al., 1994), potentially to provide yeast, no alteration in vaginal temperature, serum amino acids required for synthesis of acute-phase haptoglobin, cortisol, NEFA, or neutrophil func- proteins from hepatocytes (Reeds et  al., 1994). tionality was observed. Glucocorticoids have also been reported to have Conflict of interest statement: None declared. catabolic effects on tissues, increasing proteolysis and lipolysis, and increasing NEFA and urea N ACKNOWLEDGMENTS concentrations in blood (Brockman and Laarveld, The authors acknowledge the technical support 1986; Elsasser et  al., 1997). However, previous of J.  W. Dailey, J.  R. Carroll, and R.  Buchanan. research comparing cattle fed yeast cell wall prod- Research was funded by Phileo Lesaffre Animal ucts to a negative control reported no differences Care, Milwaukee, WI. Mention of trade names in urea N when cattle were challenged with LPS or commercial products in this article is solely for (Sanchez et al., 2014). Increased serum urea N con- the purpose of providing specific information and centrations in the CON treatment in the current does not imply recommendation or endorsement by study support the hypothesis that yeast supple- the U.S. Department of Agriculture (USDA). The mentation may be modulating the immune system USDA prohibits discrimination in all its programs in a manner that requires decreased inflammatory and activities on the basis of race, color, national response and thereby decreased lean tissue catabol- origin, age, disability, and where applicable, sex, ism. However, this hypothesis is not supported by the marital status, familial status, parental status, alteration of any immune variables measured in the religion, sexual orientation, genetic information, current study. Although a reduction in serum urea political beliefs, reprisal, or because all or part of N could result in improved performance in cattle an individual’s income is derived from any pub- supplemented with yeast and exposed to an immu- lic assistance program. (Not all prohibited bases nological insult, previous studies have reported apply to all programs.) Persons with disabilities mixed results in live performance when cattle are who require alternative means for communication supplemented with yeast products. Specifically, of program information (Braille, large print, audio- yeast cell wall supplementation tended to increase tape, etc.) should contact USDA’s TARGET Center average daily gain  (ADG) over 14 d following an at (202) 720-2600 (voice and TDD). To file a com- LPS challenge, although performance in the study plaint of discrimination, write to USDA, Director, was measured only on 24 animals (Burdick Sanchez Office of Civil Rights, 1400 Independence Avenue, et al., 2014). However, Finck et al. (2014) reported S.W., Washington, DC 20250-9410, or call (800) no difference in live feedlot performance when cat- 795-3272 (voice) or (202) 720-6382 (TDD). USDA tle were supplemented with a yeast cell wall prod- is an equal opportunity provider and employer. uct without an immunological challenge but with a trend toward decreased morbidity in cattle supple- mented with yeast. It is therefore unknown if the LITERATURE CITED change in metabolism in cattle supplemented with Akramiene, D., A.  Kondrotas, J.  Didziapetriene, and yeast in the current trial may carry over to live per- E. Kevelaitis. 2007. Effects of beta-glucans on the immune formance and clinical health differences when cat- system. Medicina (Kaunas) 43:597–606. doi:10.3390/ medicina43080076 tle are exposed to a natural immunological insult. Broadway, P. R., J. A. Carroll, and N. C. Sanchez. 2015. Live Further research may help elucidate more exact yeast and yeast cell wall supplements enhance immune performance differences and if yeast supplementa- function and performance in food-producing livestock: tion may be more beneficial in certain populations a review. Microorganisms 3:417–427. doi:10.3390/ of cattle where increased morbidity is expected. microorganisms3030417 Results of this trial indicate that alterations to Brockman, R. P., and B. Laarveld. 1986. Hormonal regulation of metabolism in ruminants; a review. Livest. Prod. Sci. the immune response to a BRD challenge when cat- 14:313–334. doi:10.1016/0301-6226(86)90012-6 tle are supplemented with combination live yeast Buchanan, J . B., E.  Peloso, and E.  Satinoff. 2003. Thermoregulatory and yeast cell wall may be minimal, while some and metabolic changes during fever in young and old rats. aspects of the metabolic response may be affected. Am. J.  Physiol. Regul. Integr. Comp. Physiol. 285:R1165– Specifically, these data suggest that serum urea N R1169. doi:10.1152/ajpregu.00238.2003 Buhman, M. J., L. J. Perino, M. L. Galyean, T. E. Wittum, T. could be reduced when cattle are supplemented Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 13 H.  Montgomery, and R. S.  Swingle. 2000. Association Hardardottir, I., C.  Grünfeld, and K. R.  Feingold. 1994. between changes in eating and drinking behaviors and Effects of endotoxin and cytokines on lipid metabolism. respiratory tract disease in newly arrived calves at a Curr. Opin. Lipidol. 5:207–215. feedlot. Am. J.  Vet. Res. 61:1163–1168. doi:10.2460/ Jericho, K. W., and E. V. Langford. 1978. Pneumonia in calves ajvr.2000.61.1163 produced with aerosols of bovine herpesvirus 1 and Burdick, N. C., J. A.  Carroll, J. W.  Dailey, R. D.  Randel, S. Pasteurella haemolytica. Can. J. Comp. Med. 42:269–277. M.  Falkenberg, and T. B.  Schmidt. 2011. Development Keyser, S. A., J. P. McMeniman, D. R. Smith, J. C. MacDonald, of a self-contained, indwelling vaginal temperature probe and M. L. Galyean. 2007. Effects of Saccharomyces cerevi- for use in cattle research. J. Thermal. Biol. 37:339–343. siae subspecies boulardii CNCM I-1079 on feed intake by doi:10.1016/j.jtherbio.2011.10.007 healthy beef cattle treated with orfenicol fl and on health Burdick Sanchez, N. C., T. R.  Young, J. A.  Carroll, J. and performance of newly received beef heifers. J. Anim. R.  Corley, R. J.  Rathmann, and B. J.  Johnson. 2013. 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Types and costs of respiratory disease treat- gen metabolism and hormonal responses of growing ments in U.S.  feedlots. Fort Collins (CO): USDA, beef steers. J. Anim. Sci. 87:3656–3668. doi:10.2527/ Animal and Plant Health Inspection Service, Veterinary jas.2009-2011 Services, Center for Epidemiology and Animal Health, Webel, D. M., B. N. Finck, D. H. Baker, and R. W. Johnson. National Animal Health Monitoring System. Available 1997. Time course of increased plasma cytokines, cortisol, from https://www.aphis.usda.gov/animal_health/nahms/ and urea nitrogen in pigs following intraperitoneal injec- feedlot/downloads/ feedlot2011/Feed11_is_RespDis.pdf. tion of lipopolysaccharide. J. Anim. Sci. 75:1514–1520. Accessed August 2017. doi:10.2527/1997.7561514x USDA. 2013b. Feedlot 2011 part IV: health and health man- Zaworski, E. M., C. M.  Shriver-Munsch, N. A.  Fadden, W. agement on U.S.  feedlots with a capacity of 1,000 or K. Sanchez, I. Yoon, and G. Bobe. 2014. Effects of feeding more head. Fort Collins (CO): USDA, Animal and Plant various dosages of Saccharomyces cerevisiae fermentation Health Inspection Service, Veterinary Services, Center product in transition dairy cows. J. Dairy Sci. 97:3081– for Epidemiology and Animal Health, National Animal 3098. doi:10.3168/jds.2013-7692 Translate basic science to industry innovation http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Translational Animal Science Oxford University Press

Immune and metabolic responses of beef heifers supplemented with Saccharomyces cerevisiae to a combined viral-bacterial respiratory disease challenge

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Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers supplemented with Saccharomyces cerevisiae to a combined viral-bacterial respiratory disease challenge † † †, ‡ Alyssa B. Word,*, P. Rand Broadway, Nicole C. Burdick Sanchez, Shelby L. Roberts, ‡ || $ $ John T. Richeson, Yu L. Liang,* Ben P. Holland, Matt D. Cravey, Jimmie R. Corley, †,1 Michael A. Ballou,* and Jeffery A. Carroll *Department of Animal and Food Sciences, Texas Tech University, Lubbock, TX 79409; Livestock Issues Research Unit, USDA-ARS, Lubbock, TX 79403; Department of Agricultural Sciences, West Texas A&M || $ University, Canyon, TX 79016; Cactus Feeders, Amarillo, TX 79106; and Phileo Lesaffre Animal Care, Milwaukee, WI 53214 ABSTRACT: Two treatments were evaluated in heif- at 0, 1, 2, 3, 4, 5, 6, 7, 8, 12, 24, 36, 48, 60, and 72 h ers to determine the effects of a yeast supplement (serum isolation) relative to M.  haemolytica chal- on immune and metabolic responses to a combined lenge (0 h). Data were analyzed using the MIXED (tandem viral-bacterial) respiratory disease chal- procedure of SAS specific for repeated measures with lenge. Thirty-two beef heifers (325  ±  20.1  kg BW) fixed effects of treatment, time, and the treatment × were selected from a larger population previously time interaction. Vaginal temperature and cortisol assigned to one of two treatments: Control (CON), concentrations were similar between treatments (P receiving no yeast supplement in the diet, or yeast ≥ 0.39). Although total leukocyte count following (YST), CON diet plus a combination live yeast BHV-1 challenge was similar between treatments −1 −1 (2.5 g·heifer ·d ) and yeast cell wall (2.5 g·heif- (P = 0.21), there was a tendency (P = 0.07) for CON −1 −1 er ·d ) supplement (Phileo Lesaffre Animal Care, heifers to have greater neutrophil counts than YST Milwaukee, WI). Heifers were maintained on treat- heifers. Serum haptoglobin concentration was sim- ments for 31 d prior to the challenge. On day −3 all ilar between treatments (P = 0.13). Heifers in the heifers were fitted with an indwelling vaginal temper - YST treatment had similar serum glucose concen- ature recording device, received an intranasal chal- trations (P = 0.25) and decreased serum concentra- lenge with 2  ×  10 plaque-forming units of bovine tions of urea nitrogen compared to CON (P = 0.03). herpesvirus-1 (BHV-1), and placed in outdoor pens. Dietary treatment did not affect serum nonesterified On day 0, all heifers were fitted with an indwelling fatty acid concentrations (P  =  0.37). Nasal lesion jugular catheter, challenged intratracheally with an score severity (0–4) tended (P = 0.07) to be decreased average dose of 3.0 × 10 colony-forming units (cfu) in YST compared to CON (2.5 vs. 3.19  ±  0.26), of Mannheimia haemolytica in 100 mL media, and while water intake tended to be increased in YST were transferred into individual stanchions in an (P  =  0.06). Feeding a yeast supplement had little enclosed, environmentally controlled barn. Whole effect on the acute-phase response but improved blood samples were collected at −72 h and at 0, 2, metabolic outcomes in heifers during a respiratory 4, 6, 8, 12, 24, 36, 48, 60, and 72 h (hematology) and disease challenge. Key words: feedlot health, immune response, metabolic response, respiratory disease challenge, yeast Published by Oxford University Press on behalf of the American Society of Animal Science 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 (http://www.nationalarchives.gov.uk/doc/open-government-licence/version/2/). Transl. Anim. Sci. 2018.XX:XX–XX doi: 10.1093/tas/txy117 Corresponding author: Jeff.Carroll@ars.usda.gov Received August 20, 2018. Accepted November 5, 2018. 1 Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 2 Word et al. INTRODUCTION Committee of the Livestock Issues Research Unit (LIRU IACUC #1605F). Bovine respiratory disease (BRD) is the lead- Yeast additive was a combination yeast cell ing cause of morbidity and mortality in U.S. feed- wall and live yeast product developed from a lots (USDA, 2013a), with 16% of cattle requiring primary S.  cerevisiae yeast strain. Thirty-two BRD treatment during the feeding period (USDA, British crossbred heifers were obtained from a 2013b). Losses in live performance or carcass value commercial feedlot in the Texas panhandle and may be experience by cattle diagnosed with BRD transported approximately 112 km to the USDA- even after clinical signs subside (Duff and Galyean, ARS Livestock Issues Research Unit’s Research 2007). While BRD is a multifaceted disease, sev- Complex in New Deal, TX. Two treatments were eral known viral and bacterial pathogens have been evaluated: 1)  Control (CON) receiving no yeast reported to be causal factors, including bovine additive in the diet, or 2) CON diet plus 2.5 g·heif- herpesvirus-1 (BHV-1) and Mannheimia haemolyt- −1 −1 −1 −1 er ·d live yeast and 2.5 g·heifer ·d yeast cell ica (Duff and Galyean, 2007). Currently, 59% of −1 −1 wall, dosed to 8 g·heifer ·d with carrier (YST, feedlots treat at least some cattle with metaphylaxis Phileo Lesaffre Animal Care, Milwaukee, WI). The to control BRD (USDA APHIS, 2013b), a process live yeast was fed to 25 × 10 colony-forming units that is under scrutiny for the judicious use of anti- −1 −1 (cfu)·heifer ·d . Heifers were chosen from a larger microbials (Dennis et  al., 2018). Methods to pre- herd of 560 heifers per treatment which had been vent or control BRD are therefore needed. received at a commercial feeding facility 35 d prior Yeast supplementation, specifically to transport to the USDA facilities. Processing at Saccharomyces cerevisiae supplementation, may the commercial feeding facility included individ- serve as a means of altering beef cattle response to ual identification with uniquely numbered ear tags, BRD during the feeding period (Finck et al., 2014). treatment with an endectocide (Cydectin Injectable, Yeast cell wall contains β-glucans that have been Bayer Animal Health, Whippany, NJ), vaccina- reported to activate macrophage and neutrophil tion against viral diseases (Vista 5 SQ, Merck function in mice (Akramiene et  al., 2007). These Animal Health, Summit, NJ) and clostridial dis- β-glucans are associated with improved immune eases (Ultrabac 7, Zoetis, Florham Park, NJ), and function (Broadway et al., 2015) and therefore health administered an anabolic implant (Revalor-IH, of newly received feedlot cattle (Keyser et al., 2007). Merck Animal Health). Heifers were selected for Live yeast and yeast cell wall supplements may each the current trial from the larger herd in order to bind pathogenic microorganisms such as Salmonella select a sample with similar phenotype. Selection or Escherichia coli and prevent colonization of these criteria included black hided cattle without visi- bacteria in the gastrointestinal tract (Perez-Sotelo ble Brahman influence, cattle with a similar tem- et  al., 2005; Posadas et al., 2017). While the mech- perament using the pen and chute scoring system anism of action is not completely understood, yeast described by King et al. (2006), uniformity of BW, supplements have altered morbidity and mortality in and average serum antibody titer against BHV-1 feedlot cattle (Keyser et al., 2007; Finck et al., 2014), of 16 for each treatment (Texas A&M Veterinary and may reduce immune response severity and neg- Diagnostic Laboratory, Amarillo, TX). Blood for ative metabolic outcomes (Burdick Sanchez et  al., serum was collected on a larger sample of cattle at 2013, 2014). Therefore, the objective of the current the commercial facility and analyzed for serum anti- study was to evaluate the effects of a supplement body titer against BHV-1 prior to arrival at USDA containing live S. cerevisiae and S. cerevisiae cell wall facilities. The scoring system outlined by King et al. components on the immune and metabolic outcomes (2006) was used to assign cattle to subjective pen of feedlot heifers administered a combined viral and scores prior to being processed where 1  =  walks bacterial BRD challenge. The experimental hypothe- slowly, can be approached slowly, not excited by sis was that supplementing heifers with yeast for 31 d humans; 2 = runs along fences, stands in corner if prior to the BRD challenge would improve immune humans stay away; 3 = runs along fences, head up and metabolic responses to a BRD challenge. and will run if humans approach but stops before hitting gates and fences; 4 = runs, stays in back of MATERIALS AND METHODS group, head high and aware of humans, may run into fences and gates; 5 = excited, runs into fences All experimental procedures were in com- or anything in path. Chute scores were assigned as pliance with the Guide for the Care and Use of cattle were processed where 1 = calm, no movement; Agricultural Animals in Research and Teaching and 2  =  slightly restless; 3  =  squirming, occasionally approved by the Institutional Animal Care and Use Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 3 shaking the chute; 4  =  continuous, very rigorous finish diet for RAMP at 15% intervals every 2 to 4 movement and shaking of the chute; 5  =  rearing, d. Feed was transported every 3 d from commercial twisting of the body and struggling violently. Pen facilities to USDA facilities after cattle were trans- and chute score were then averaged to assign each ported, and stored in a tarp-covered trailer inside a heifer a temperament score, and animals were cho- covered, temperature-controlled barn. Average ini- sen based on an average score of less than 3.  All tial BW of the cattle transported to USDA facilities heifers selected had not received treatment for was 325 ± 20.1 kg. Following arrival at the USDA clinical BRD during the feeding period. All heif- facility, heifers were allowed to rest overnight in dirt ers had been randomized to treatment group and pens (7.6  ×  18.3 m) and were maintained on the maintained on respective treatments (n  =  16 per respective treatment diets previously assigned at the treatment) for 31 d prior to arrival at the USDA commercial feeding location, with ad libitum access facilities for a commercial research trial evaluating to water. On study day −3, heifers were weighed the same yeast product used in the current study. and fitted with a vaginal temperature recording At the commercial facility, heifers were fed 100% device. Briefly, a temperature sensor (Star-ODDi RAMP (Cargill Corn Milling, Bovina, TX) and DST micro-T; MeterMall USA, Marysville, OH) transitioned to the same diet fed at the USDA facil- was secured into a blank controlled internal drug ities (Table  1) by incremental substitution of the release (CIDR) device (Pfizer Animal Health, Sterling, CO) as described by Burdick et al. (2011), Table 1. Ingredient formulation and analyzed com- which was then placed using a CIDR applicator position of finish diets into the vagina of each heifer. Vaginal tempera- ture was measured every 5 min from insertion until Finish diet formula- the completion of the study. A  nasal lesion score tions (% of DM) was also recorded at this time where 0  =  absence Ingredient of lesions; 1  =  less than 10% coverage of the vis- Corn, steam flaked 58.5 Corn distillers grain, wet 17.1 ible naris; 2  =  11% to 25% coverage; 3  =  26% to Wet corn gluten feed 16.1 50% coverage; and 4 = 50% or greater coverage of Corn stalks, chopped 7.2 the visible naris. All heifers were challenged intra- Fat 1.1 nasally at this time with approximately 2  ×  10 Additives plaque-forming units (pfu) of BHV-1. For the Vitamin A, IU/kg 2,645 BHV-1 dose, a single vial of BHV-1 was diluted to Vitamin D, IU/kg 264.6 a final concentration of 1 × 10 pfu/mL, and then −1 −1 Melengesterol acetate, mg·heifer ·d 0.40 1  mL of diluted virus was administered per naris Monensin, mg/kg 46.85 in each heifer using a syringe and a nasal atomiza- Tylosin, mg/kg 10.69 tion device. Whole blood was collected into a 4-mL 4 5 Analyzed composition (% of DM) CON YST tube containing 7.2  mg K EDTA (Vacutainer; Dry matter 60.3 60.8 Becton, Dickinson, and Company, Franklin Lakes, Crude protein 15.1 15.3 NJ) and blood for serum isolation collected into Equivalent crude protein 1.0 1.0 a 9-mL tube (Vacutainer; Becton, Dickinson, and Neutral detergent fiber 20.8 20.9 Company, Franklin Lakes, NJ) containing no addi- Fat 5.2 5.2 tive via jugular venipuncture prior to challenge. Ca 0.74 0.70 All heifers were then returned to the outdoor pens P 0.51 0.51 and were monitored daily for clinical symptoms of Mg 0.24 0.24 BRD. Indwelling vaginal temperature recording K 0.81 0.82 devices were removed on study day 3. S 0.25 0.25 The morning of study day 0, heifers were fitted Sweet Bran wet corn gluten feed (Cargill Corn Milling, Bovina, TX) with an indwelling jugular catheter. Whole blood with added calcium carbonate (4% as fed), salt (1.8%), urea (1.1%), and blood for serum was collected via the jugu- and trace mineral premix (0.2%). lar catheter and heifers were challenged with log- Rumensin 90, Elanco Animal Health. Tylosin 100, Elanco Animal Health. arithmic phase culture M.  haemolytica in 100  mL Reported by Servi-Tech Laboratories, Amarillo, TX. Values are media. Four batches of M. haemolytica were made means (n = 7). and heifers received the challenge in blocks of eight Treatments were: 1) negative control (CON) fed a standard finish- heifers to ensure that each received log phase cul- −1 −1 ing diet, or 2)  YST, fed the same finishing diet with 2.5 g·heifer ·d −1 −1 ture. Mannheimia haemolytica titers (cfu counts) live yeast and 2.5 g·heifer ·d yeast cell wall (Phileo Lesaffre Animal Care, Milwaukee, WI). were determined by serial dilution and plating Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 4 Word et al. immediately prior to the first animal receiving the using a commercially available enzyme immuno- intratracheal challenge and immediately following assay kit according to the manufacturer’s directions the eighth (final) animal challenged for each batch. (Arbor Assays, Ann Arbor, MI) by compari- Each batch was measured on a UV visible spectro- son of unknowns to standard curves generated photometer at 590 nm to a transmittance between with known concentrations of cortisol. Minimum 62% and 68%. Based on this, the average dose of detectable cortisol concentration was 0.4  ng/mL, the four batches was 3.0 × 10 cfu of M. haemolyt- and the intra- and inter-assay coefficients of var - ica. Each heifer was challenged with the prepared iation were 10.6% and 4.2%, respectively. Serum M.  haemolytica via intratracheal injection using a haptoglobin concentrations were also determined 16 gauge, 25.4 mm needle and two 60 mL syringes. using a commercially available enzyme immuno- Heifers were then moved to individual stalls (2.28 assay kit according to the manufacturer’s direc- m in length, 0.76 m in width, and 1.67 m in height). tions (Immunology Consultants Laboratory, Inc., Heifers were fed a complete finishing diet (Table 1) Portland, OR). Intra- and inter-assay coefficients once daily ad libitum such that each heifer was of variation were 6.0% and 15.3%, respectively. offered 4.5 kg of fresh feed each morning and orts Glucose concentrations were determined by were discarded (Table  1). Yeast supplement was modification of the enzymatic Autokit glucose hand mixed into the daily ration while heifers were (Wako Pure Chemical Industries, Chuo-Ku, Osaka, in the stanchions to the appropriate treatments. Japan) to fit a 96-well format, where 300  µL of pre- Prior to the immunological challenge, no feed was pared working solution was added to 2 µL of serum discarded, although yeast treatment may have been or prepared standards in a 96-well plate. Plates were included in feed that was refused by heifers dur- incubated at 3 °C for 5 min and then read using a ing the immunological challenge and subsequently plate reader at 505  nm. Concentration of glucose discarded. Individual water intake was measured was determined by comparing unknown samples to from 0 to 72 h while heifers were housed in individ- a standard curve of known glucose concentrations. ual stanchions via a Suevia Cup (QC Supply Inc., Minimum detectable concentration was 3.8 mg/dL Schuyler, NE). Whole blood was collected in 4-mL and intra- and inter-assay coefficients of variation tube containing 7.2  mg K EDTA at 0, 2, 4, 6, 8, were 7.4% and 10.7%, respectively. 12, 24, 36, 48, 60, and 72  h post-M.  haemolytica Serum nonesterified fatty acid (NEFA) concen- challenge via the jugular catheter. Blood for serum trations were determined by modification of the was collected in 9-mL Sarstedt tubes containing no enzymatic HR Series NEFA-HR (2) assay (Wako additive (Sarstedt, Inc., Newton, NC) every hour Diagnostics, Richmond, VA) to fit a 96-well format until hour 8, at 12 h, and then every 12 h until 72 h where 200 µL of the Color Reagent A were added via the jugular catheter. Blood for serum was incu- to 5 µL of serum or prepared standards in a 96-well bated at room temperature for 30 min and then cen- plate. Plates were incubated at 37 °C for 5 min and trifuged at 1,500 × g for 20 min at 4 °C and serum then the absorbance was read using a spectropho- removed and frozen at −80 °C. Following the col- tometer at 550 nm. Next, 100 µL of Color Reagent lection of the 72  h sample, heifers were weighed, B was added to all wells on the 96-well plate. Plates jugular catheters were removed, and all heifers were incubated for an additional 5  min and read were treated with florfenicol (Nuflor Gold, Merck for a second time using a plate reader at 550  nm. Animal Health, Madison, NJ) by subcutaneous A  final absorbance was obtained by subtracting injection at 40  mg florfenicol/kg body weight to the first reading, which was multiplied by a factor treat the known bacterial (M.  haemolytica) infec- of 0.67 to account for changes in volume, from the tion that had been administered to the animals. second reading. The final absorbance values were Whole blood samples were analyzed for hema- used for all calculations. Concentrations of NEFA tology, including: total leukocyte counts, leukocyte were determined by comparing unknown samples differential, hematocrit, and hemoglobin using to a standard curve of known NEFA concentra- an IDEXX Procyte Dx Hematology Analyzer tions. The minimum detectable concentration (IDEXX Labs, Westbrook, ME) with bovine-spe- was 0.021  mmol/L and the intra- and inter-assay cific algorithms. Whole blood was also collected coefficients of variation were 8.8% and 10.5%, in heparinized tubes at −72, 0, and 48 h relative to respectively. M.  haemolytica challenge and analyzed to deter- Concentrations of serum urea nitrogen were mine polymorphonuclear (PMN) leukocyte activity. determined by a colorimetric assay according to the All serum analyses were performed in duplicate. manufacturer’s directions (K024-H1; Arbor Assays, Serum cortisol concentrations were determined Ann Arbor, MI) by comparison of unknowns to Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 5 standard curves generated with known concentra- sample collected at 0 h was analyzed due to differ- tions of urea nitrogen. The minimum detectable ences between treatment at 0 h. Nasal lesion scores concentration was 0.093  mg/dL and intra- and were analyzed using the GLIMMIX procedure of inter-assay coefficients of variation were 12.8% and SAS with fixed effects of treatment, time, and the 8.7%, respectively. treatment × time interaction. All data presented are Neutrophil functionality was determined by as LSM ± SEM with P ≤ 0.05 considered significant the phagocytic and oxidative burst capacity against and 0.05 < P ≤ 0.10 considered a tendency. an environmental E.  coli as well as the surface expression of the adhesion molecule, CD62L (i.e., RESULTS L-selectin), as described by Obeidat et  al. (2013). No treatment × time interaction occurred Briefly, oxidative burst intensity and phagocytic (P  =  0.84) for vaginal temperature, and tempera- activity was determined by incubating 200  µL of ture was similar (P = 0.39) between CON and YST whole blood in an ice bath and then combining (Figure  1; 39.4  ±  0.08 vs. 39.3  ±  0.08  °C, respec- with 40 µL each of 100 µM dihydrorhodamine and tively). Vaginal temperature increased (P  <  0.001) heat-killed E. coli at 1 × 10 cells per mL. Samples for 10  h in both treatments following the BHV- were incubated in a 38.5 °C water bath for 10 min, 1/M. haemolytica challenge with a peak of 40.2 °C then subsequently placed in an ice bath for 15 min occurring at 10  h. Water intake, and hematologi- to stop the reaction, hypotonically lysed, and then cal measures are reported in Table 2. There was no washed with ice cold phosphate-buffered saline treatment × time interaction (P  =  0.52) for water (PBS). A  BD Accuri flow cytometer was used to intake, and total water intake tended to be greater analyze leukocytes, and neutrophils were gated on (P = 0.06) in the YST treatment compared to CON the scatterplot of forward scatter × side scatter. (676  ±  32.3 vs. 588  ±  32.3  mL/h, respectively). Data are reported as the percentage of neutrophils Water intake fluctuated over time following viral that were positive for phagocytosis and oxida- challenge (P < 0.01). tive burst as well as the mean fluorescence inten- No treatment × time interaction occurred sity of the positive populations. Negative controls (P  =  0.98) for serum cortisol concentration included E.  coli only, remained on ice throughout (Figure  2). Serum cortisol was similar (P  =  0.90) the dihydrorhodamine, and incubated with remain- between treatments (20.7 ± 1.14 vs. 20.5 ± 1.14 ng/ ing samples. The surface expression of L-selectin mL for CON and YST, respectively). Serum cortisol was determined by incubating 50  µL of whole concentration was greatest at time of M. haemolyt- blood with anti-bovine CDL62L (monoclonal ica challenge and decreased over time (P < 0.01). No antibody IgG1-isotype in the mouse; VMRD Inc., treatment × time interaction (P = 0.23) occurred for Pullman, WA) at a final dilution of 5  µg/mL for 1 h any hematological measure. Hematological meas- in an ice bath, then hypotonically lysed and rinsed ures, except for neutrophil concentrations, were with PBS. The pellet was resuspended in fluoresce- not different (P ≥ 0.16) between treatments. Total in-labeled secondary antibody and incubated on ice neutrophil concentration tended (P  =  0.07) to be for 1 h, then washed twice using PBS and analyzed greater in CON heifers (6.4 ± 0.39 vs. 5.4 ± 0.37 10 using flow cytometry as described above. The nega- cells per µL, respectively). Number of neutrophils in tive control was secondary antibody only. Data are circulation increased following live pathogen chal- reported as the mean fluorescence intensity of each lenge until hour 8 and then decreased (P  <  0.01). sample. No treatment × time interaction occurred (P ≥ Vaginal temperature data were averaged into 0.47) for any measure of neutrophil functionality. 1-h intervals for analysis. Hematological, meta- Neutrophil phagocytosis, oxidative burst inten- bolic, and temperature data were analyzed using sity, and expression of L-selectin were not differ- the MIXED procedure of SAS specific for repeated ent between treatments (P ≥ 0.13). Oxidative burst measures (SAS Institute Inc., Cary, NC) with fixed intensity and expression of L-selectin increased in effects of treatment, time, and the treatment × both treatments over time (P  <  0.001). There was time interaction. The autoregressive (1) covariance no treatment × time interaction (P  =  0.94) for structure for the within-subject measurement was serum haptoglobin concentration. Haptoglobin used in all models except for vaginal temperature was not different (P  =  0.13) between treatments data, where the compound symmetry covariance (15,396.2  ±  1,631.7 vs. 11,757.3  ±  1,631.7  µg/ structure was used. Covariance structures were dL; P  =  0.13; Figure  3), although haptoglobin chosen based on the smaller Bayesian Information increased (time effect: P < 0.01) in both treatments Criterion. For serum glucose, change relative to the Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 6 Word et al. CON YST Ambient 40.4 39.6 40.2 39.4 39.2 39.8 39.6 38.8 39.4 39.2 38.6 38.4 38.8 38.2 38.6 38.4 38.2 37.8 -4 -1 2 5 8 11 14 17 20 23 26 29 32 35 38 41 44 47 50 53 56 59 62 65 68 71 Hour relative to M. haemolytica challenge Figure  1. Effect of yeast supplementation on vaginal temperature response in beef heifers (n  =  16/trt). Heifers were fed one of two dietary −1 −1 treatments: 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 −1 −1 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged 8 7 intranasally with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means. There was no treatment × time interaction (P = 0.84) and vaginal temperature was not affected by dietary treatment (P = 0.39), although temperature decreased over time (P < 0.01). Treatment means were 39.4 ± 0.08 for CON and 39.3 ± 0.08 °C for YST. SEM = 0.084. Table  2. Effect of yeast supplementation on vaginal temperature, water intake, nasal lesion score, serum and hematology variables, and neutrophil functionality in feedlot heifers administered a respiratory disease challenge Treatment Item CON YST SEM P-value Vaginal temperature, °C 39.4 39.3 0.08 0.39 Water intake, mL/h 588 676 32.3 0.06 Serum haptoglobin, µg/dL 15,396 11,757 1,631.7 0.13 Serum cortisol, ng/mL 20.7 20.5 1.14 0.90 Lymphocytes, 10 /µL 4.65 4.59 0.26 0.86 Neutrophils, 10 /µL 6.39 5.37 0.39 0.07 Neutrophil:Lymphocyte 1.50 1.35 0.12 0.36 Platelets, 10 /µL 438.8 399.3 30.5 0.36 Red blood cells, 10 /µL 7.60 7.29 0.15 0.17 Eosonophils, 10 /µL 0.18 0.17 0.03 0.72 Hematocrit, % 34.3 33.8 0.48 0.43 Hemoglobin, g/dL 11.2 11.0 0.13 0.16 Monocytes, 10 /µL 1.60 1.64 0.073 0.65 Neutrophil oxidative burst intensity, GMFI 119,898 135,696 7,227.5 0.13 PMN phagocytosis, GMFI 47,013 45,867 2,650.8 0.76 L-Selectin expression, GMFI 98,030 103,914 3,966.3 0.30 Heifers were fed one of two dietary treatments: 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with −1 −1 −1 −1 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) 31 d prior to immunological challenge (YST). Whole blood was collected every 2 h from 0 to 8 h and every 12 h from 12 to 72 h for hematology, and every 1 h from 0 to 2 h and every 12 h from 12 to 72 h for serum analysis. Represents treatment P-value. All treatment × time interactions were P ≥ 0.19. Geometric mean florescence intensity (GMFI) for neutrophil oxidative burst intensity, phagocytosis, and L-selectin expression. Whole blood was collected −72, 0, and 48 h relative to Mannheimia haemolytica immunological challenge. and remained so through the final sampling time There was a trend (P = 0.04) for a treatment × point at 72 h following the BHV-1/M. haemolytica time interaction for serum glucose where CON challenge. heifers had decreased serum glucose at 1  h and Translate basic science to industry innovation Vaginal temperature (°C) Ambient temperature (°C) Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 7 CON YST 01234567 8122436486072 Hour relative to M. haemolytica challenge Figure 2. Effect of yeast supplementation on serum cortisol response in beef heifers (n = 16/trt). Heifers were fed one of two dietary treatments: −1 −1 −1 −1 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged intranasally 8 7 with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means ± SEM. There was no treatment × time interaction (P = 0.98) and serum cortisol was not affected by dietary treatment (P = 0.90), although serum cortisol decreased over time (P < 0.01) as cattle adapted to stanchions. CON YST -10000 0 1234567 8122436486072 Hour relative to M. haemolytica challenge Figure  3. Effect of yeast supplementation on serum haptoglobin response in beef heifers (n  =  16/trt). Heifers were fed one of two dietary −1 −1 treatments: 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 −1 −1 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged 8 7 intranasally with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means ± SEM. There was no treatment × time interaction (P = 0.94) and serum haptoglobin was not affected by dietary treatment (P = 0.13), although serum haptoglobin increased over time (P < 0.01). remained so until 6 h following BHV-1/M. haemo- YST, respectively; Figure  5). Serum urea N was lytica challenge, at which time the treatments were greater (P = 0.03) in the CON treatment compared similar. Serum glucose concentration was similar to YST (11.8 ± 0.53 vs. 10.1 ± 0.53 mg/dL, respec- between treatments (P  =  0.25; Figure  4). There tively; Figure 6). Serum urea N generally increased was no treatment × time interaction (P ≥ 0.65) for over time following BHV-1/M.  haemolytica chal- serum NEFA or urea N concentrations. Serum lenge (P  <  0.001). Nasal lesion scores recorded 6 NEFA increased in both treatments from 0 to 12 h, d following BHV-1 challenge tended (P = 0.07) to and subsequently decreased (time P < 0.01), but be more severe in CON heifers compared to YST was not different (P  =  0.37) between treatments (Figure 7). However, heifers in both treatments pre- (0.15 ± 0.01 vs. 0.14 ± 0.01 mmol/L for CON and sented with nasal lesions of varying severity. Translate basic science to industry innovation Serum haptoglobin (µg/dL ) Cortisol concentration, ng/mL Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 8 Word et al. -20 CON -40 YST -60 -80 -100 -120 -140 12345678 12 24 36 48 60 72 Hour relative to M. haemolytica challenge Figure 4. Effect of yeast supplementation on serum glucose response in beef heifers (n = 16/trt). Heifers were fed one of two dietary treatments: −1 −1 −1 −1 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). Data presented as least squares means ± SEM and 0 h was used as a covariate in the analysis. All heifers were challenged intranasally with 2 × 10 plaque-forming units bovine herpesvirus-1 (BHV-1) at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. There was a tendency for a treatment × time interaction (P = 0.04) such that CON heifers had decreased serum glucose at 1 h and remained so until 6 h following BHV-1/M. haemolytica. Serum glucose was similar between dietary treatments (P = 0.25). 0.3 0.25 0.2 0.15 CON YST 0.1 0.05 01234567 8122436486072 Hour relative to Mannheimia haemolytica challenge Figure 5. Effect of yeast supplementation on serum NEFA response in beef heifers (n = 16/trt). Heifers were fed one of two dietary treatments: −1 −1 −1 −1 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged intranasally 8 7 with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means ± SEM. Serum NEFA was not affected by dietary treatment (P = 0.37) and there was no treatment × time interaction (P = 0.88). DISCUSSION at 0  h. Peak temperatures (40.2  °C in both treat- ments) were similar to the threshold (40 °C) febrile Dietary treatment did not affect vaginal tem- response reported by Perino and Apley (1998) for perature in the current study. In contrast, Finck BRD treatment in feedlots. Average temperature et al. (2014) reported decreased rectal temperature in each treatment group in this trial was near the following an lipopolysaccharide (LPS) challenge threshold for clinical illness outlined by Duff and in steers fed yeast cell wall or a combination live Galyean (2007), and is similar to a febrile response and yeast cell wall compared to a negative con- from which cellular immunological responses could trol. Vaginal temperature increased in all treat- ments when calves were experimentally challenged be anticipated (Thomson et al., 1975). Although Translate basic science to industry innovation Serum non-esterfied fatty acid (mmol/L) Change in glucose concentration (mg/dL) Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 9 CON YST 0 12345678 12 24 36 48 60 72 Hour relative to Mannheimia haemolytica challenge Figure  6. Effect of yeast supplementation on serum urea nitrogen response in beef heifers (n  =  16/trt). Heifers were fed one of two dietary −1 −1 treatments: 1) negative control (CON), fed a standard feedlot diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 −1 −1 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). All heifers were challenged 8 7 intranasally with 2 × 10 plaque-forming units bovine herpesvirus-1 at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h. Data presented as least squares means ± SEM. Serum urea nitrogen was decreased in YEAST compared to CON (P = 0.03) and there was no treatment × time interaction (P = 0.65). the current study collected vaginal temperature, meeting outlined requirements for water intake rectal and vaginal temperatures have been reported in finishing cattle (NRC, 2000). However, hemat- to be highly correlated during immunological ocrit percentage and other hematological measure- challenges (Burdick et al., 2011; Falkenberg et al., ments were similar between treatments and were 2014). Jericho and Langford (1978) established an within the range of what is considered normal in interaction between BHV-1 and M.  haemolytica beef cattle (Radostits et  al., 2000) so water intake in BRD when they reported fibrous pneumonic is not expected to have affected the interpretation lesions similar to lesions occurring in field BRD of hematological or other measures reported in calves experimentally challenged with these path- this trial. ogens, dependent on a 3- to 5-d interval between Nasal lesion scores tended to be more severe viral and bacterial inoculation similar to the in the CON treatment. Ulcerated nasal mucosa is interval used in the current trial. Vaginal temper- a symptom of respiratory infection with BHV-1, ature also fluctuated within each day, which was and leads to the more severe “red nose” infection expected. Although heifers were housed in an envir- frequently associated with infectious bovine rhi- onmentally controlled barn, daily ambient temper- notracheitis (Nandi et  al., 2009). Heifers in both ature fluctuations occurred, which paired with the treatment groups exhibited nasal lesion scores ≥1 circadian rhythm of vaginal temperature may have and had lesions of varying severity present; there- resulted in the daily fluctuations observed. Burdick fore, the BHV-1 challenge did successfully elicit et al. (2011) reported that the vaginal temperature clinical signs of an immune response in both treat- devices used in the current trial are capable of meas- ment groups. uring the circadian rhythm in vaginal temperature. Dietary treatment did not affect serum cortisol Water intake was greater in the YST treatment concentration in the current study. This response compared to CON. Previous literature has reported is similar to the serum cortisol response observed that frequency and duration of water intake was by Burdick Sanchez et al. (2013), who reported no similar (Sowell et al., 1999) or increased (Buhman difference when beef heifers were supplemented et  al., 2000) in feedlot cattle that were clinically with yeast cell wall compared to a negative con- ill compared to healthy cattle. Water is required trol and challenged with LPS. In contrast, Finck for multiple maintenance functions including reg- et al. (2014) reported that feeding combination live ulation of body temperature, metabolism, and yeast and yeast cell wall to beef steers decreased transportation of cells through the bloodstream, serum cortisol concentrations compared to a neg- including immune cells. In terms of total daily ative control following an LPS challenge. In the intake, heifers in both treatment groups were not current study, increased cortisol production due Translate basic science to industry innovation Serum urea nitrogen (mg/dL) Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 10 Word et al. CON 3 YST 0 1234 Nasal Lesion Score Figure 7. Effect of yeast supplementation on nasal lesion scores (0–4) in beef heifers (n = 16/trt) All heifers were challenged intranasally with 8 7 2 × 10 plaque-forming units bovine herpesvirus-1 (BHV-1) at −144 h and 3 × 10 colony-forming units Mannheimia haemolytica at 0 h and scores were collected 72 h following BHV-1 challenge. Heifers were fed one of two dietary treatments: 1) negative control (CON), fed a standard feedlot −1 −1 −1 −1 diet, or 2) the same standard feedlot diet with 2.5 g·heifer ·d live yeast and 2.5 g·heifer ·d yeast cell wall product (Phileo Lesaffre Animal Care, Milwaukee, WI) for 31 d prior to challenge (YST). Score was determined according to the following criteria: 0 = absence of lesions; 1 = less than 10% coverage of the visible naris; 2 = 11% to 25% coverage; 3 = 26% to 50% coverage; and 4 = 50% or greater coverage of the visible naris. Data presented as number of animals receiving a score within each category. Nasal lesion scores tended (P = 0.07) to be more severe in CON compared to YST. to stress during processing and administration of greater probability for long-term tissue damage the bacterial challenge marked a rapid increase in as neutrophils undergo apoptosis or migrate into circulating cortisol in both treatments. However, peripheral tissue, expression of L-selectin was not serum cortisol concentrations in both treatments different between treatments in the current trial. were greatest immediately following M.  haemo- Therefore, the tendency for increased circulating lytica challenge and decreased at each subsequent neutrophils was not explained by decreased chemo- time point. Such a response suggests that heifers taxis mediated by L-selectin. Results for both may have been stressed due to handling involved treatments agree with the literature as expression with catheterization and challenge, but serum cor- of L-selectin increased over time in conjunction tisol concentrations decreased as heifers became with decreased circulating cortisol (Burton et  al., adapted to the stanchions. Therefore, there appears 1995). In contrast to Akramiene et al. (2007), PMN to be no cortisol response directly to the viral-bac- phagocytosis and oxidative burst intensity in the terial challenge. current trial were not different between treatments A tendency for greater circulating neutrophil but generally increased following M.  haemolytica concentrations occurred in CON compared to YST challenge as neutrophils became active in tissue in the current trial. While the mode of action of and began phagocytizing and ultimately destroying yeast products has not been clearly defined, cell bacterial pathogens. wall of S.  cerevisiae contains β-glucans that have Serum haptoglobin concentrations were similar also been reported to enhance phagocytic activity between CON and YST treatments following the of neutrophils in vitro (Akramiene et  al., 2007). BHV-1/M.  haemolytica challenge. Haptoglobin is Neutrophil concentration in circulation has also an acute-phase protein secreted from hepatocytes been reported to increase in the presence of glu- during inflammation, is undetectable in healthy cocorticoids, as L-selectin expression and there- calves, and could take up to 4 to 8 d after live fore chemotaxis of neutrophils into peripheral pathogen infection to be detectable in sick cattle tissues decreases in the presence of glucocorticoids (Ganheim et  al., 2003). In the current study, data (Burton et  al., 1995). However, these neutrophils were only collected for 6 d following BHV-1 inoc- may exhibit a “rebound effect” after circulating ulation, which may not have been enough time to glucocorticoids decrease that allow chemotaxis measure peak haptoglobin response. Future stud- into peripheral tissues, increasing phagocytic activ- ies should collect serum haptoglobin concentra- ity and thereby lung tissue damage in the case of tions for up to 14 d, as concentrations may begin to BRD-affected calves (Burton et  al., 2005). While return to normal after 13 d (Ganheim et al., 2003). increased circulating neutrophils may indicate Acute-phase protein production from hepatocytes Translate basic science to industry innovation Number of heifers scored in each category, n Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 Immune and metabolic responses of beef heifers 11 is stimulated by pro-inflammatory cytokines, spe- Immunological insults initially induce hyperg- cifically IL-6 (Naka et al., 2002). Burdick Sanchez lycemia, as has been demonstrated during the stress et  al. (2013) reported that serum IL-6 concentra- response, and subsequently cause hypoglycemia tion was decreased in cattle supplemented with a in response to increased metabolic demands for similar yeast cell wall product when compared to a energy. Waggoner et  al. (2009) reported that beef negative control following LPS challenge. In con- steers challenged with LPS initially increased above trast, Zaworski et al. (2014) reported no difference and subsequently decreased below the serum glu- in serum haptoglobin concentration postpartum cose concentration of an unchallenged cohort, sug- in dairy cows supplemented with S.  cerevisiae. gesting an initial increase during the inflammatory However, these authors did report increased Serum response and a decrease as cattle use the energy Amyloid A  concentration 1 d after calving in to deal with the immunological challenge, which cows supplemented with S.  cerevisiae, which they could explain the rapid increase at 5  h and subse- hypothesize may be beneficial after calving because quent decrease reported in the current trial. When acute-phase protein production creates a negative testing for a metabolite that could aid in the predic- feedback loop that downregulates the production tion of BRD outcomes, Montgomery et al. (2009) of pro-inflammatory cytokines. reported a linear decrease in blood glucose concen- Immune responses to an immunological insult tration measured on-arrival as subsequent number require large amounts of energy and potentially of BRD treatments during the receiving period change nutrient partitioning. A  1  °C increase in increased. The authors hypothesized cattle with body temperature increases resting metabolic rate decreased blood glucose on-arrival that were later by 10% to 20% in mice (Buchanan et al., 2003), and treated for BRD may have been exposed to path- further energy is required to produce acute-phase ogens prior to arrival and experienced hypoglyce- proteins and other mediators of inflammation and mia on-arrival because they were already fighting the immune response (Carroll and Forsberg, 2007). disease. Serum glucose concentration in the current In the current study, there was a treatment effect trial was decreased in the CON treatment from 1 to for serum glucose concentrations where serum glu- 5 h compared to the YST treatment, in line with the cose was greater in the YST treatment compared initial decrease that Montgomery et al. (2009) and to CON. The increase in glucose concentration in Waggoner et al. (2009) have suggested to be indic- the YST group may imply that a greater amount of ative of disease risk and indicates that cattle were readily available glucose was being utilized in the already responding to the BHV-1 challenge prior to CON treatment compared to the YST, potentially the M. haemolytica challenge administered at 0 h. to meet increased metabolic requirements of the Serum NEFA concentrations were similar immune system. Cytokines were reported to stimu- between CON and YST treatments. In contrast, late hepatic gluconeogenesis while increasing over- previous studies have reported both decreased all utilization of glucose in mice and pigs (Lang IL-6 production and subsequent decreased serum and Spitzer, 1987; Webel et  al., 1997), although NEFA concentration in cattle fed yeast cell wall this proposed mechanism cannot be confirmed as compared to a negative control when each were cytokines were not measured in the current study. challenged with LPS (Burdick Sanchez et  al., When challenging with LPS and feeding a yeast cell 2013, 2014). Exposure to endotoxin induced wall, Burdick Sanchez et al. (2014) reported no dif- hypertriglyceridemia by inhibiting lipoprotein ference in serum glucose concentration compared lipase activity and inducing hepatic fatty acid syn- to a negative control, although insulin concentra- thesis in rats, which is stimulated in part by pro- tion was greatest in cattle supplemented with yeast duction of the pro-inflammatory cytokine IL-6 cell wall, which is in contrast with results of the cur- (Hardardottir et  al., 1994). The authors explain rent trial. However, Zaworski et al. (2014) reported benefits of these metabolic changes include meet- a tendency for increased serum glucose and serum ing increased metabolic needs and the ability of urea nitrogen postpartum in dairy cows fed a lipoproteins to both bind endotoxin and inhibit S.  cerevisiae strain, which the authors propose to viral replication. An increase in serum NEFA in be a faster transition out of a negative energy bal- all treatments following BHV-1/M.  haemolytica ance postpartum. Metabolic results of that study challenge in the current trial could be the mixed could be in agreement with results of the current result of cattle in both treatments needing to meet study, where increased serum glucose concentration the energetic requirements of the immune system is considered desirable because cattle are not parti- and altered need for antiviral mechanisms follow- tioning that energy elsewhere. ing the viral challenge. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txy117/5200779 by Ed 'DeepDyve' Gillespie user on 27 November 2018 12 Word et al. Serum urea N was increased in the CON with yeast and exposed to an immunological chal- treatment compared to YST in the current study. lenge. While nasal lesion scores tended to be less Pro-inflammatory cytokines have been reported severe and neutrophil concentration tended to be to increase catabolism of lean tissue in pigs decreased when cattle were supplemented with (Hardardottir et  al., 1994), potentially to provide yeast, no alteration in vaginal temperature, serum amino acids required for synthesis of acute-phase haptoglobin, cortisol, NEFA, or neutrophil func- proteins from hepatocytes (Reeds et  al., 1994). tionality was observed. Glucocorticoids have also been reported to have Conflict of interest statement: None declared. catabolic effects on tissues, increasing proteolysis and lipolysis, and increasing NEFA and urea N ACKNOWLEDGMENTS concentrations in blood (Brockman and Laarveld, The authors acknowledge the technical support 1986; Elsasser et  al., 1997). However, previous of J.  W. Dailey, J.  R. Carroll, and R.  Buchanan. research comparing cattle fed yeast cell wall prod- Research was funded by Phileo Lesaffre Animal ucts to a negative control reported no differences Care, Milwaukee, WI. Mention of trade names in urea N when cattle were challenged with LPS or commercial products in this article is solely for (Sanchez et al., 2014). Increased serum urea N con- the purpose of providing specific information and centrations in the CON treatment in the current does not imply recommendation or endorsement by study support the hypothesis that yeast supple- the U.S. Department of Agriculture (USDA). The mentation may be modulating the immune system USDA prohibits discrimination in all its programs in a manner that requires decreased inflammatory and activities on the basis of race, color, national response and thereby decreased lean tissue catabol- origin, age, disability, and where applicable, sex, ism. However, this hypothesis is not supported by the marital status, familial status, parental status, alteration of any immune variables measured in the religion, sexual orientation, genetic information, current study. Although a reduction in serum urea political beliefs, reprisal, or because all or part of N could result in improved performance in cattle an individual’s income is derived from any pub- supplemented with yeast and exposed to an immu- lic assistance program. (Not all prohibited bases nological insult, previous studies have reported apply to all programs.) Persons with disabilities mixed results in live performance when cattle are who require alternative means for communication supplemented with yeast products. Specifically, of program information (Braille, large print, audio- yeast cell wall supplementation tended to increase tape, etc.) should contact USDA’s TARGET Center average daily gain  (ADG) over 14 d following an at (202) 720-2600 (voice and TDD). To file a com- LPS challenge, although performance in the study plaint of discrimination, write to USDA, Director, was measured only on 24 animals (Burdick Sanchez Office of Civil Rights, 1400 Independence Avenue, et al., 2014). However, Finck et al. (2014) reported S.W., Washington, DC 20250-9410, or call (800) no difference in live feedlot performance when cat- 795-3272 (voice) or (202) 720-6382 (TDD). USDA tle were supplemented with a yeast cell wall prod- is an equal opportunity provider and employer. uct without an immunological challenge but with a trend toward decreased morbidity in cattle supple- mented with yeast. It is therefore unknown if the LITERATURE CITED change in metabolism in cattle supplemented with Akramiene, D., A.  Kondrotas, J.  Didziapetriene, and yeast in the current trial may carry over to live per- E. Kevelaitis. 2007. Effects of beta-glucans on the immune formance and clinical health differences when cat- system. 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Published: Nov 23, 2018

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