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ARS Home » Midwest Area » Ames, Iowa » National Laboratory for Agriculture and The Environment » Agroecosystems Management Research » Research » Research Project #433200

Research Project: Reducing Production Losses due to Oxidative Stress and Bacterial Pathogens in Swine

Location: Agroecosystems Management Research

2018 Annual Report


Objectives
The objectives of the project are to develop an understanding of the interrelationships between non-antibiotic feed additives and pathogen translocation and shedding in growing pigs, obtain critical measures of oxidative stress in growing pigs and reproducing swine, and develop interventions to reduce or prevent pathogen colonization and disease in swine in an effort to maximize production efficiency but minimize environmental impact. Objective 1: Evaluate alternatives to antibiotics (butyric acid, resistant starch, inulin, etc.) for maintaining growth performance and reducing intestinal bacterial translocation and shedding in growing pigs. Objective 2: Determine the inherent variation in oxidative stress measures in breeding and lactating gilts, and correlate to measures of sow lifetime productivity. Objective 3: Identify markers associated with oxidative stress and correlate to changes in pig growth and feed intake, using peroxidized soybean oil as the inducer of oxidative stress. Objective 4: Determine whether vaccination of swine with a Salmonella DIVA vaccine can prevent/reduce colonization and improve growth following transmission of Salmonella from actively shedding pigs.


Approach
Alternatives to antibiotics for growing pigs will be assessed through the evaluation of compounds which have the potential to affect gastrointestinal function and microbial ecology which would, therefore, affect pig performance. Compounds to be evaluated include resistant starch, soluble dietary fiber, short- and medium-chain fatty acids, phytogenics, inorganic minerals, and beta-glucans; all of which have been suggested to affect gastrointestinal function and microbial ecology. Determination of the inherent variation in oxidative stress measures in breeding and lactating gilts will be assessed by collecting biological samples from gestating and lactating sows at 4 critical time points during these reproduction phases, and measuring key oxidative stress parameters (DNA, protein, and lipid damage) as well as antioxidant status (plasma vitamin E). In growing pigs, identification of markers associated with oxidative stress and impact on pig performance will be assessed by feeding peroxidized soybean oil to nursery, grower, or finishing pigs. Peroxidized soybean oil will be generated by heating soybean oil at 45°C for 288 h, 90°C for 72 h, or 180°C for 6 h, in comparison to unheated (22.5°C) soybean oil. Oxidative stress will be assessed measuring key oxidative stress parameters (e.g., DNA, protein, and lipid damage) as well as antioxidant status (e.g., plasma vitamin E) while performance effects will be measured by growth over a predetermined period. An attenuated Salmonella vaccine was previously designed and constructed to provide broad protection against numerous Salmonella serovars in food-producing animals. A Salmonella transmission trial will be performed in swine to determine whether vaccination against Salmonella can prevent or reduce Salmonella colonization and improve growth performance following exposure to pigs actively shedding Salmonella.


Progress Report
Research on feeding peroxidized soybean oil to mice and growing pigs indicated that consumption of peroxided lipids resulted in a reduction in animal growth rate, increased measures of oxidative stress, and suggested that metabolism of the peroxidized soybean oil resulted in excretion of urinary compounds that are specifically associated with metabolizing peroxidized soybean oil in the animal. In addition, this research indicated that consumption of mildly peroxidized soybean oil in finish pigs had no impact on carcass quality or on subsequent bacon quality. Research on how to feed pigs in the absence of antibiotics was initiated with a focus on compounds that increase the production of butyric acid in the large intestine. Non-typhoidal Salmonella are a leading cause of foodborne disease in the U.S. and Salmonella enterica serovar I 4,[5],12,i:- has emerged as the fifth most common Salmonella serovar. In 2015, a foodborne outbreak due to multidrug-resistant (MDR) serovar I 4,[5],12,i:- was linked to pork with 188 human infections and 30 hospitalizations. To gain a better understanding of the emergence of MDR serovar I 4,[5],12,i:- in swine production, we are characterized the genome of a pork outbreak-associated isolate FSIS1503788. The genome of MDR serovar I 4,[5],12,i:- isolate FSIS1503788 was shown to have two genetic insertions that encode genes for resistance to multiple antimicrobials (ampicillin, streptomycin, sulfisoxazole, and tetracycline) and heavy metals (mercury, copper, zinc, and arsenic). An isogenic mutant of FSIS1503788 was constructed that had reduced growth in the presence of copper or arsenic, indicating that the presence of the corresponding metal resistance genes in wildtype FSIS1503788 increases pathogen survival in environments containing copper and arsenic. The acquisition of genetic regions that confer resistance to antimicrobials and metals may have provided a colonization or environmental advantage to increase the prevalence of serovar I 4,[5],12,i:- in animal production. Furthermore, the use of certain antimicrobials or metals in swine production may have unintended consequences by providing selective pressure to promote colonization by MDR Salmonella serovar I 4,[5],12,i:-.


Accomplishments
1. Ionophore feeding has limited effects on energy and nutrient digestion in growing pigs and does not appear to affect manure composition or gas emissions in manure generated from finishing pigs. Ionophores, such as narasin, are antibiotic-like compounds which are known to affect microbial ecology in the gastrointestinal tract of growing pigs. In the current research, feeding an ionophore to pigs improved energy and nutrient digestion in nursery pigs, but did not affect energy or nutrient digestion in growing or finishing pigs. In addition, feeding narasin to finishing pigs had negligible effects on manure composition and did not affect manure gas emissions of volatile fatty acids, ammonia, or greenhouse gasses. Because this research demonstrated that there was only a limited effect of a dietary ionophore on energy of nutrient digestion in pigs and, generally, no effect on manure composition and subsequent gas emissions, it is of importance to the swine industry in showing the limited value of this compound to affect pig performance and subsequent manure composition and gas emissions.

2. Outbreak-associated, multidrug-resistant (MDR) Salmonella Heidelberg efficiently colonizes young turkeys. In 2011, multidrug-resistant (MDR) Salmonella Heidelberg was associated with a foodborne illness outbreak from ground turkey that sickened 136 individuals and resulted in 1 death; 36 million pounds of ground turkey were recalled, one of the largest meat recalls in U.S. history. ARS researchers in Ames, Iowa, inoculated turkeys with a MDR Salmonella Heidelberg isolate associated with the 2011 ground turkey outbreak and determined gastrointestinal colonization a week later. Salmonella Heidelberg colonization in young turkeys was 100-fold higher than the inoculation dose and pen-mates (that were not directly inoculated) were colonized to the same extent as if they had also been inoculated with Salmonella. This indicates that Salmonella transmission between pen-mates is efficient and young turkeys are vulnerable to colonization with MDR Salmonella Heidelberg. This research provides knowledge concerning the ability of outbreak-associated MDR Salmonella Heidelberg to colonize commercial turkeys and indicates that preventative strategies must target young turkeys that are susceptible to colonization by Salmonella.


Review Publications
Kerr, B.J., Trabue, S.L., van Weelden, M., Andersen, D., Pepple, L. 2018. Impact of narasin on manure composition and microbial ecology, and gas emissions from finishing pigs fed either a corn-soybean meal or a corn-soybean meal-dried distillers grains with solubles diets. Journal of Animal Science. 96:1317-1329. https://doi.org/10.1093/jas/sky053.
Mauch, E.D., Young, J.M., Serao, N.V.L., Hsu, W.L., Patience, J.F., Kerr, B.J., Weber, T.E., Gabler, N.K., Dekkers, J.C.M. 2018. Effect of lower-energy, higher-fiber diets on pigs divergently selected for residual feed intake when fed higher-energy, lower-fiber diets. Journal of Animal Science. 96:1221-1236. https://doi.org/10.1093/jas/sky065.
Yu, D.Y., Lindemann, M.D., Quant, A.D., Jang, Y.D., Payne, R.L., Kerr, B.J. 2017. Antibiotic inclusion in the diet did not alter the standardized ileal digestible tryptophan to lysine ratio for growing pigs. Journal of Animal Science. 95(12):5516-5523. https://doi.org/10.2527/jas2017.1982.
Lindblom, S., Gabler, N., Kerr, B.J. 2018. Influence of feeding thermally peroxidized soybean oil on growth performance, digestibility, and gut integrity in growing pigs. Journal of Animal Science. 96(2):558-569. https://doi.org/10.1093/jas/sky004.
Lindblom, S., Gabler, N., Dilger, R., Olson, Z.F., Loving, C.L., Kerr, B.J. 2018. Influence of feeding thermally peroxidized soybean oil on oxidative status in growing pigs. Journal of Animal Science. 96:545-557. https://doi.org/10.1093/jas/sky005.
Holman, D., Bearson, S.M., Bearson, B.L., Brunelle, B.W. 2018. Chlortetracycline and florfenicol induce expression of genes associated with pathogenicity in multidrug-resistant Salmonella enterica serovar Typhimurium. Gut Pathogens. 10:10. https://doi.org/10.1186/s13099-018-0236-y.
Shippy, D.C., Bearson, B.L., Holman, D.B., Brunelle, B.W., Allen, H.K., Bearson, S.M. 2018. Porcine response to a multidrug-resistant Salmonella enterica serovar I 4,[5],12:i:- outbreak isolate. Foodborne Pathogens and Disease. 15(5):253-261. https://doi.org/10.1089/fpd.2017.2378.
Brunelle, B.W., Bearson, B.L., Bearson, S.M., Casey, T. 2017. Multidrug-resistant Salmonella enterica serovar Typhimurium isolates are resistant to antibiotics that influence their swimming and swarming motility. mSphere. 2:e00306-17. https://doi.10.1128/mSphere.00306-17.
Bearson, B.L., Bearson, S.M., Looft, T., Cai, G., Shippy, D.C. 2017. Characterization of a multidrug-resistant Salmonella enterica serovar Heidelberg outbreak strain in commercial turkeys: Colonization, transmission, and host transcriptional response. Frontiers in Veterinary Science. 4:156. https://doi.org/10.3389/fvets.2017.00156.
Soupir, M.L., Hoover, N.L., Moorman, T.B., Bearson, B.L., Law, J.Y. 2018. Impact of temperature and hydraulic retention time on pathogen and nutrient removal in woodchip bioreactors. Ecological Engineering. 112:153-157. https://doi.org/10.1016/j.ecoleng.2017.12.005.
Kerr, B.J., Trabue, S.L., Andersen, D.S. 2017. Narasin effects on energy, nutrient, and fiber digestibility in corn-soybean meal or corn-soybean meal-dried distillers grains with soluble diets fed to 16-, 92-, and 141-kg pigs. Journal of Animal Science. 95(9):4030-4036. https://doi.org/10.2527/jas.2017.1732.
Murugesan, G., Kerr, B.J., Persia, M. 2017. Energy content of select dietary supplemental lipids for broilers, turkeys, and laying hens. Journal of Applied Poultry Research. 26:536-547.
Schweer, W.P., Patience, J.F., Burrough, E.R., Kerr, B.J., Gabler, N.K. 2018. Impact of PRRSV infection and dietary soybean meal on ileal amino acid digestibility and endogenous amino acid losses in growing pigs. Journal of Animal Science. 96:1846-1859. https://doi.org/10.1093/jas/sky093.
Wang, L., Yao, D., Urriola, P., Hanson, A., Saqui, M., Kerr, B.J., Shurson, G., Chen, C. 2018. Identification of activation of tryptophan-NAD+ pathway as a central metabolic response to thermally oxidized oil through metabolomics-guided biochemical analysis. Journal of Nutritional Biochemistry. 57:255-267.
Andersen, D.S., Yang, F., Trabue, S.L., Kerr, B.J., Howe, A.S. 2018. Narasin as manure additive to reduce methane production from swine manure. Transactions of the ASABE. 61(3):943-953. https://doi.org/10.13031/trans.12568.
Overholt, M.F., Kim, G., Boler, D., Kerr, B.J., Dilger, A. 2018. Influence of feeding thermally peroxidized soybean oil to finishing pigs on carcass characteristics, loin quality, and shelf-life of loin chops. Journal of Animal Science. 96:2710-2722.
Overholt, M.F., Lowell, J., Kim, G., Boler, D., Kerr, B.J., Dilger, A. 2018. Influence of feeding thermally peroxidized soybean oil to finishing barrows on processing characteristics and shelf-life of commercially manufactured bacon. Journal of Animal Science. 96:2723-2733.
Overholt, M.F., Dilger, A.C., Boler, D.D., Kerr, B.J. 2018. Influence of feeding thermally peroxidized soybean oil on growth performance, digestibility, and gut integrity in finishing pigs. Journal of Animal Science. 96:2789-2803.